Insects: A Very Short Introduction

VERY SHORT INTRODUCTIONS are for anyone wanting a stimulating and accessible way into a new subject. They are written by experts, and have been translated into more than 45 different languages.

 The series began in 1995, and now covers a wide variety of topics in every discipline. The VSI library currently contains over 700 volumes—a Very Short Introduction to everything from Psychology and Philosophy of Science to American History and Relativity—and continues to grow in every subject area.

Very Short Introductions available now:

ABOLITIONISM Richard S. Newman

THE ABRAHAMIC RELIGIONS Charles L. Cohen

ACCOUNTING Christopher Nobes

ADOLESCENCE Peter K. Smith

THEODOR W. ADORNO Andrew Bowie

ADVERTISING Winston Fletcher

AERIAL WARFARE Frank Ledwidge

AESTHETICS Bence Nanay

AFRICAN AMERICAN RELIGION Eddie S. Glaude Jr

AFRICAN HISTORY John Parker and Richard Rathbone

AFRICAN POLITICS Ian Taylor

AFRICAN RELIGIONS Jacob K. Olupona

AGEING Nancy A. Pachana

AGNOSTICISM Robin Le Poidevin

AGRICULTURE Paul Brassley and Richard Soffe

ALEXANDER THE GREAT Hugh Bowden

ALGEBRA Peter M. Higgins

AMERICAN BUSINESS HISTORY Walter A. Friedman

AMERICAN CULTURAL HISTORY Eric Avila

AMERICAN FOREIGN RELATIONS Andrew Preston

AMERICAN HISTORY Paul S. Boyer

AMERICAN IMMIGRATION David A. Gerber

AMERICAN INTELLECTUAL HISTORY Jennifer Ratner-Rosenhagen

AMERICAN LEGAL HISTORY G. Edward White

AMERICAN MILITARY HISTORY Joseph T. Glatthaar

AMERICAN NAVAL HISTORY Craig L. Symonds

AMERICAN POETRY David Caplan

AMERICAN POLITICAL HISTORY Donald Critchlow

AMERICAN POLITICAL PARTIES AND ELECTIONS L. Sandy Maisel

AMERICAN POLITICS Richard M. Valelly

THE AMERICAN PRESIDENCY Charles O. Jones

THE AMERICAN REVOLUTION Robert J. Allison

AMERICAN SLAVERY Heather Andrea Williams

THE AMERICAN SOUTH Charles Reagan Wilson

THE AMERICAN WEST Stephen Aron

AMERICAN WOMEN’S HISTORY Susan Ware

AMPHIBIANS T. S. Kemp

ANAESTHESIA Aidan O’Donnell

ANALYTIC PHILOSOPHY Michael Beaney

ANARCHISM Colin Ward

ANCIENT ASSYRIA Karen Radner

ANCIENT EGYPT Ian Shaw

ANCIENT EGYPTIAN ART AND ARCHITECTURE Christina Riggs

ANCIENT GREECE Paul Cartledge

THE ANCIENT NEAR EAST Amanda H. Podany

ANCIENT PHILOSOPHY Julia Annas

ANCIENT WARFARE Harry Sidebottom

ANGELS David Albert Jones

ANGLICANISM Mark Chapman

THE ANGLO-SAXON AGE John Blair

ANIMAL BEHAVIOUR Tristram D. Wyatt

THE ANIMAL KINGDOM Peter Holland

ANIMAL RIGHTS David DeGrazia

THE ANTARCTIC Klaus Dodds

ANTHROPOCENE Erle C. Ellis

ANTISEMITISM Steven Beller

ANXIETY Daniel Freeman and Jason Freeman

THE APOCRYPHAL GOSPELS Paul Foster

APPLIED MATHEMATICS Alain Goriely

THOMAS AQUINAS Fergus Kerr

ARBITRATION Thomas Schultz and Thomas Grant

ARCHAEOLOGY Paul Bahn

ARCHITECTURE Andrew Ballantyne

THE ARCTIC Klaus Dodds and Jamie Woodward

ARISTOCRACY William Doyle

ARISTOTLE Jonathan Barnes

ART HISTORY Dana Arnold

ART THEORY Cynthia Freeland

ARTIFICIAL INTELLIGENCE Margaret A. Boden

ASIAN AMERICAN HISTORY Madeline Y. Hsu

ASTROBIOLOGY David C. Catling

ASTROPHYSICS James Binney

ATHEISM Julian Baggini

THE ATMOSPHERE Paul I. Palmer

AUGUSTINE Henry Chadwick

JANE AUSTEN Tom Keymer

AUSTRALIA Kenneth Morgan

AUTISM Uta Frith

AUTOBIOGRAPHY Laura Marcus

THE AVANT GARDE David Cottington

THE AZTECS Davíd Carrasco

BABYLONIA Trevor Bryce

BACTERIA Sebastian G. B. Amyes

BANKING John Goddard and John O. S. Wilson

BARTHES Jonathan Culler

THE BEATS David Sterritt

BEAUTY Roger Scruton

LUDWIG VAN BEETHOVEN Mark Evan Bonds

BEHAVIOURAL ECONOMICS Michelle Baddeley

BESTSELLERS John Sutherland

THE BIBLE John Riches

BIBLICAL ARCHAEOLOGY Eric H. Cline

BIG DATA Dawn E. Holmes

BIOCHEMISTRY Mark Lorch

BIOGEOGRAPHY Mark V. Lomolino

BIOGRAPHY Hermione Lee

BIOMETRICS Michael Fairhurst

ELIZABETH BISHOP Jonathan F. S. Post

BLACK HOLES Katherine Blundell

BLASPHEMY Yvonne Sherwood

BLOOD Chris Cooper

THE BLUES Elijah Wald

THE BODY Chris Shilling

THE BOOK OF COMMON PRAYER Brian Cummings

THE BOOK OF MORMON Terryl Givens

BORDERS Alexander C. Diener and Joshua Hagen

THE BRAIN Michael O’Shea

BRANDING Robert Jones

THE BRICS Andrew F. Cooper

THE BRITISH CONSTITUTION Martin Loughlin

THE BRITISH EMPIRE Ashley Jackson

BRITISH POLITICS Tony Wright

BUDDHA Michael Carrithers

BUDDHISM Damien Keown

BUDDHIST ETHICS Damien Keown

BYZANTIUM Peter Sarris

CALVINISM Jon Balserak

ALBERT CAMUS Oliver Gloag

CANADA Donald Wright

CANCER Nicholas James

CAPITALISM James Fulcher

CATHOLICISM Gerald O’Collins

CAUSATION Stephen Mumford and Rani Lill Anjum

THE CELL Terence Allen and Graham Cowling

THE CELTS Barry Cunliffe

CHAOS Leonard Smith

GEOFFREY CHAUCER David Wallace

CHEMISTRY Peter Atkins

CHILD PSYCHOLOGY Usha Goswami

CHILDREN’S LITERATURE Kimberley Reynolds

CHINESE LITERATURE Sabina Knight

CHOICE THEORY Michael Allingham

CHRISTIAN ART Beth Williamson

CHRISTIAN ETHICS D. Stephen Long

CHRISTIANITY Linda Woodhead

CIRCADIAN RHYTHMS Russell Foster and Leon Kreitzman

CITIZENSHIP Richard Bellamy

CITY PLANNING Carl Abbott

CIVIL ENGINEERING David Muir Wood

CLASSICAL LITERATURE William Allan

CLASSICAL MYTHOLOGY Helen Morales

CLASSICS Mary Beard and John Henderson

CLAUSEWITZ Michael Howard

CLIMATE Mark Maslin

CLIMATE CHANGE Mark Maslin

CLINICAL PSYCHOLOGY Susan Llewelyn and Katie Aafjes-van Doorn

COGNITIVE BEHAVIOURAL THERAPY Freda McManus

COGNITIVE NEUROSCIENCE Richard Passingham

THE COLD WAR Robert J. McMahon

COLONIAL AMERICA Alan Taylor

COLONIAL LATIN AMERICAN LITERATURE Rolena Adorno

COMBINATORICS Robin Wilson

COMEDY Matthew Bevis

COMMUNISM Leslie Holmes

COMPARATIVE LITERATURE Ben Hutchinson

COMPETITION AND ANTITRUST LAW Ariel Ezrachi

COMPLEXITY John H. Holland

THE COMPUTER Darrel Ince

COMPUTER SCIENCE Subrata Dasgupta

CONCENTRATION CAMPS Dan Stone

CONFUCIANISM Daniel K. Gardner

THE CONQUISTADORS Matthew Restall and Felipe Fernández-Armesto

CONSCIENCE Paul Strohm

CONSCIOUSNESS Susan Blackmore

CONTEMPORARY ART Julian Stallabrass

CONTEMPORARY FICTION Robert Eaglestone

CONTINENTAL PHILOSOPHY Simon Critchley

COPERNICUS Owen Gingerich

CORAL REEFS Charles Sheppard

CORPORATE SOCIAL RESPONSIBILITY Jeremy Moon

CORRUPTION Leslie Holmes

COSMOLOGY Peter Coles

COUNTRY MUSIC Richard Carlin

CREATIVITY Vlad Glăveanu

CRIME FICTION Richard Bradford

CRIMINAL JUSTICE Julian V. Roberts

CRIMINOLOGY Tim Newburn

CRITICAL THEORY Stephen Eric Bronner

THE CRUSADES Christopher Tyerman

CRYPTOGRAPHY Fred Piper and Sean Murphy

CRYSTALLOGRAPHY A. M. Glazer

THE CULTURAL REVOLUTION Richard Curt Kraus

DADA AND SURREALISM David Hopkins

DANTE Peter Hainsworth and David Robey

DARWIN Jonathan Howard

THE DEAD SEA SCROLLS Timothy H. Lim

DECADENCE David Weir

DECOLONIZATION Dane Kennedy

DEMENTIA Kathleen Taylor

DEMOCRACY Bernard Crick

DEMOGRAPHY Sarah Harper

DEPRESSION Jan Scott and Mary Jane Tacchi

DERRIDA Simon Glendinning

DESCARTES Tom Sorell

DESERTS Nick Middleton

DESIGN John Heskett

DEVELOPMENT Ian Goldin

DEVELOPMENTAL BIOLOGY Lewis Wolpert

THE DEVIL Darren Oldridge

DIASPORA Kevin Kenny

CHARLES DICKENS Jenny Hartley

DICTIONARIES Lynda Mugglestone

DINOSAURS David Norman

DIPLOMATIC HISTORY Joseph M. Siracusa

DOCUMENTARY FILM Patricia Aufderheide

DREAMING J. Allan Hobson

DRUGS Les Iversen

DRUIDS Barry Cunliffe

DYNASTY Jeroen Duindam

DYSLEXIA Margaret J. Snowling

EARLY MUSIC Thomas Forrest Kelly

THE EARTH Martin Redfern

EARTH SYSTEM SCIENCE Tim Lenton

ECOLOGY Jaboury Ghazoul

ECONOMICS Partha Dasgupta

EDUCATION Gary Thomas

EGYPTIAN MYTH Geraldine Pinch

EIGHTEENTH‑CENTURY BRITAIN Paul Langford

THE ELEMENTS Philip Ball

EMOTION Dylan Evans

EMPIRE Stephen Howe

EMPLOYMENT LAW David Cabrelli

ENERGY SYSTEMS Nick Jenkins

ENGELS Terrell Carver

ENGINEERING David Blockley

THE ENGLISH LANGUAGE Simon Horobin

ENGLISH LITERATURE Jonathan Bate

THE ENLIGHTENMENT John Robertson

ENTREPRENEURSHIP Paul Westhead and Mike Wright

ENVIRONMENTAL ECONOMICS Stephen Smith

ENVIRONMENTAL ETHICS Robin Attfield

ENVIRONMENTAL LAW Elizabeth Fisher

ENVIRONMENTAL POLITICS Andrew Dobson

ENZYMES Paul Engel

EPICUREANISM Catherine Wilson

EPIDEMIOLOGY Rodolfo Saracci

ETHICS Simon Blackburn

ETHNOMUSICOLOGY Timothy Rice

THE ETRUSCANS Christopher Smith

EUGENICS Philippa Levine

THE EUROPEAN UNION Simon Usherwood and John Pinder

EUROPEAN UNION LAW Anthony Arnull

EVANGELICALISM John Stackhouse

EVOLUTION Brian and Deborah Charlesworth

EXISTENTIALISM Thomas Flynn

EXPLORATION Stewart A. Weaver

EXTINCTION Paul B. Wignall

THE EYE Michael Land

FAIRY TALE Marina Warner

FAMILY LAW Jonathan Herring

MICHAEL FARADAY Frank A. J. L. James

FASCISM Kevin Passmore

FASHION Rebecca Arnold

FEDERALISM Mark J. Rozell and Clyde Wilcox

FEMINISM Margaret Walters

FILM Michael Wood

FILM MUSIC Kathryn Kalinak

FILM NOIR James Naremore

FIRE Andrew C. Scott

THE FIRST WORLD WAR Michael Howard

FLUID MECHANICS Eric Lauga

FOLK MUSIC Mark Slobin

FOOD John Krebs

FORENSIC PSYCHOLOGY David Canter

FORENSIC SCIENCE Jim Fraser

FORESTS Jaboury Ghazoul

FOSSILS Keith Thomson

FOUCAULT Gary Gutting

THE FOUNDING FATHERS R. B. Bernstein

FRACTALS Kenneth Falconer

FREE SPEECH Nigel Warburton

FREE WILL Thomas Pink

FREEMASONRY Andreas Önnerfors

FRENCH LITERATURE John D. Lyons

FRENCH PHILOSOPHY Stephen Gaukroger and Knox Peden

THE FRENCH REVOLUTION William Doyle

FREUD Anthony Storr

FUNDAMENTALISM Malise Ruthven

FUNGI Nicholas P. Money

THE FUTURE Jennifer M. Gidley

GALAXIES John Gribbin

GALILEO Stillman Drake

GAME THEORY Ken Binmore

GANDHI Bhikhu Parekh

GARDEN HISTORY Gordon Campbell

GENES Jonathan Slack

GENIUS Andrew Robinson

GENOMICS John Archibald

GEOGRAPHY John Matthews and David Herbert

GEOLOGY Jan Zalasiewicz

GEOMETRY Maciej Dunajski

GEOPHYSICS William Lowrie

GEOPOLITICS Klaus Dodds

GERMAN LITERATURE Nicholas Boyle

GERMAN PHILOSOPHY Andrew Bowie

THE GHETTO Bryan Cheyette

GLACIATION David J. A. Evans

GLOBAL CATASTROPHES Bill McGuire

GLOBAL ECONOMIC HISTORY Robert C. Allen

GLOBAL ISLAM Nile Green

GLOBALIZATION Manfred B. Steger

GOD John Bowker

GOETHE Ritchie Robertson

THE GOTHIC Nick Groom

GOVERNANCE Mark Bevir

GRAVITY Timothy Clifton

THE GREAT DEPRESSION AND THE NEW DEAL Eric Rauchway

HABEAS CORPUS Amanda Tyler

HABERMAS James Gordon Finlayson

THE HABSBURG EMPIRE Martyn Rady

HAPPINESS Daniel M. Haybron

THE HARLEM RENAISSANCE Cheryl A. Wall

THE HEBREW BIBLE AS LITERATURE Tod Linafelt

HEGEL Peter Singer

HEIDEGGER Michael Inwood

THE HELLENISTIC AGE Peter Thonemann

HEREDITY John Waller

HERMENEUTICS Jens Zimmermann

HERODOTUS Jennifer T. Roberts

HIEROGLYPHS Penelope Wilson

HINDUISM Kim Knott

HISTORY John H. Arnold

THE HISTORY OF ASTRONOMY Michael Hoskin

THE HISTORY OF CHEMISTRY William H. Brock

THE HISTORY OF CHILDHOOD James Marten

THE HISTORY OF CINEMA Geoffrey Nowell-Smith

THE HISTORY OF LIFE Michael Benton

THE HISTORY OF MATHEMATICS Jacqueline Stedall

THE HISTORY OF MEDICINE William Bynum

THE HISTORY OF PHYSICS J. L. Heilbron

THE HISTORY OF POLITICAL THOUGHT Richard Whatmore

THE HISTORY OF TIME Leofranc Holford‑Strevens

HIV AND AIDS Alan Whiteside

HOBBES Richard Tuck

HOLLYWOOD Peter Decherney

THE HOLY ROMAN EMPIRE Joachim Whaley

HOME Michael Allen Fox

HOMER Barbara Graziosi

HORMONES Martin Luck

HORROR Darryl Jones

HUMAN ANATOMY Leslie Klenerman

HUMAN EVOLUTION Bernard Wood

HUMAN PHYSIOLOGY Jamie A. Davies

HUMAN RESOURCE MANAGEMENT Adrian Wilkinson

HUMAN RIGHTS Andrew Clapham

HUMANISM Stephen Law

HUME James A. Harris

HUMOUR Noël Carroll

THE ICE AGE Jamie Woodward

IDENTITY Florian Coulmas

IDEOLOGY Michael Freeden

THE IMMUNE SYSTEM Paul Klenerman

INDIAN CINEMA Ashish Rajadhyaksha

INDIAN PHILOSOPHY Sue Hamilton

THE INDUSTRIAL REVOLUTION Robert C. Allen

INFECTIOUS DISEASE Marta L. Wayne and Benjamin M. Bolker

INFINITY Ian Stewart

INFORMATION Luciano Floridi

INNOVATION Mark Dodgson and David Gann

INSECTS Simon Leather

INTELLECTUAL PROPERTY Siva Vaidhyanathan

INTELLIGENCE Ian J. Deary

INTERNATIONAL LAW Vaughan Lowe

INTERNATIONAL MIGRATION Khalid Koser

INTERNATIONAL RELATIONS Christian Reus-Smit

INTERNATIONAL SECURITY Christopher S. Browning

IRAN Ali M. Ansari

ISLAM Malise Ruthven

ISLAMIC HISTORY Adam Silverstein

ISLAMIC LAW Mashood A. Baderin

ISOTOPES Rob Ellam

ITALIAN LITERATURE Peter Hainsworth and David Robey

HENRY JAMES Susan L. Mizruchi

JESUS Richard Bauckham

JEWISH HISTORY David N. Myers

JEWISH LITERATURE Ilan Stavans

JOURNALISM Ian Hargreaves

JAMES JOYCE Colin MacCabe

JUDAISM Norman Solomon

JUNG Anthony Stevens

KABBALAH Joseph Dan

KAFKA Ritchie Robertson

KANT Roger Scruton

KEYNES Robert Skidelsky

KIERKEGAARD Patrick Gardiner

KNOWLEDGE Jennifer Nagel

THE KORAN Michael Cook

KOREA Michael J. Seth

LAKES Warwick F. Vincent

LANDSCAPE ARCHITECTURE Ian H. Thompson

LANDSCAPES AND GEOMORPHOLOGY Andrew Goudie and Heather Viles

LANGUAGES Stephen R. Anderson

LATE ANTIQUITY Gillian Clark

LAW Raymond Wacks

THE LAWS OF THERMODYNAMICS Peter Atkins

LEADERSHIP Keith Grint

LEARNING Mark Haselgrove

LEIBNIZ Maria Rosa Antognazza

C. S. LEWIS James Como

LIBERALISM Michael Freeden

LIGHT Ian Walmsley

LINCOLN Allen C. Guelzo

LINGUISTICS Peter Matthews

LITERARY THEORY Jonathan Culler

LOCKE John Dunn

LOGIC Graham Priest

LOVE Ronald de Sousa

MARTIN LUTHER Scott H. Hendrix

MACHIAVELLI Quentin Skinner

MADNESS Andrew Scull

MAGIC Owen Davies

MAGNA CARTA Nicholas Vincent

MAGNETISM Stephen Blundell

MALTHUS Donald Winch

MAMMALS T. S. Kemp

MANAGEMENT John Hendry

NELSON MANDELA Elleke Boehmer

MAO Delia Davin

MARINE BIOLOGY Philip V. Mladenov

MARKETING Kenneth Le Meunier-FitzHugh

THE MARQUIS DE SADE John Phillips

MARTYRDOM Jolyon Mitchell

MARX Peter Singer

MATERIALS Christopher Hall

MATHEMATICAL FINANCE Mark H. A. Davis

MATHEMATICS Timothy Gowers

MATTER Geoff Cottrell

THE MAYA Matthew Restall and Amara Solari

THE MEANING OF LIFE Terry Eagleton

MEASUREMENT David Hand

MEDICAL ETHICS Michael Dunn and Tony Hope

MEDICAL LAW Charles Foster

MEDIEVAL BRITAIN John Gillingham and Ralph A. Griffiths

MEDIEVAL LITERATURE Elaine Treharne

MEDIEVAL PHILOSOPHY John Marenbon

MEMORY Jonathan K. Foster

METAPHYSICS Stephen Mumford

METHODISM William J. Abraham

THE MEXICAN REVOLUTION Alan Knight

MICROBIOLOGY Nicholas P. Money

MICROECONOMICS Avinash Dixit

MICROSCOPY Terence Allen

THE MIDDLE AGES Miri Rubin

MILITARY JUSTICE Eugene R. Fidell

MILITARY STRATEGY Antulio J. Echevarria II

JOHN STUART MILL Gregory Claeys

MINERALS David Vaughan

MIRACLES Yujin Nagasawa

MODERN ARCHITECTURE Adam Sharr

MODERN ART David Cottington

MODERN BRAZIL Anthony W. Pereira

MODERN CHINA Rana Mitter

MODERN DRAMA Kirsten E. Shepherd-Barr

MODERN FRANCE Vanessa R. Schwartz

MODERN INDIA Craig Jeffrey

MODERN IRELAND Senia Pašeta

MODERN ITALY Anna Cento Bull

MODERN JAPAN Christopher Goto-Jones

MODERN LATIN AMERICAN LITERATURE Roberto González Echevarría

MODERN WAR Richard English

MODERNISM Christopher Butler

MOLECULAR BIOLOGY Aysha Divan and Janice A. Royds

MOLECULES Philip Ball

MONASTICISM Stephen J. Davis

THE MONGOLS Morris Rossabi

MONTAIGNE William M. Hamlin

MOONS David A. Rothery

MORMONISM Richard Lyman Bushman

MOUNTAINS Martin F. Price

MUHAMMAD Jonathan A. C. Brown

MULTICULTURALISM Ali Rattansi

MULTILINGUALISM John C. Maher

MUSIC Nicholas Cook

MYTH Robert A. Segal

NAPOLEON David Bell

THE NAPOLEONIC WARS Mike Rapport

NATIONALISM Steven Grosby

NATIVE AMERICAN LITERATURE Sean Teuton

NAVIGATION Jim Bennett

NAZI GERMANY Jane Caplan

NEOLIBERALISM Manfred B. Steger and Ravi K. Roy

NETWORKS Guido Caldarelli and Michele Catanzaro

THE NEW TESTAMENT Luke Timothy Johnson

THE NEW TESTAMENT AS LITERATURE Kyle Keefer

NEWTON Robert Iliffe

NIELS BOHR J. L. Heilbron

NIETZSCHE Michael Tanner

NINETEENTH‑CENTURY BRITAIN Christopher Harvie and H. C. G. Matthew

THE NORMAN CONQUEST George Garnett

NORTH AMERICAN INDIANS Theda Perdue and Michael D. Green

NORTHERN IRELAND Marc Mulholland

NOTHING Frank Close

NUCLEAR PHYSICS Frank Close

NUCLEAR POWER Maxwell Irvine

NUCLEAR WEAPONS Joseph M. Siracusa

NUMBER THEORY Robin Wilson

NUMBERS Peter M. Higgins

NUTRITION David A. Bender

OBJECTIVITY Stephen Gaukroger

OCEANS Dorrik Stow

THE OLD TESTAMENT Michael D. Coogan

THE ORCHESTRA D. Kern Holoman

ORGANIC CHEMISTRY Graham Patrick

ORGANIZATIONS Mary Jo Hatch

ORGANIZED CRIME Georgios A. Antonopoulos and Georgios Papanicolaou

ORTHODOX CHRISTIANITY A. Edward Siecienski

OVID Llewelyn Morgan

PAGANISM Owen Davies

PAKISTAN Pippa Virdee

THE PALESTINIAN-ISRAELI CONFLICT Martin Bunton

PANDEMICS Christian W. McMillen

PARTICLE PHYSICS Frank Close

PAUL E. P. Sanders

PEACE Oliver P. Richmond

PENTECOSTALISM William K. Kay

PERCEPTION Brian Rogers

THE PERIODIC TABLE Eric R. Scerri

PHILOSOPHICAL METHOD Timothy Williamson

PHILOSOPHY Edward Craig

PHILOSOPHY IN THE ISLAMIC WORLD Peter Adamson

PHILOSOPHY OF BIOLOGY Samir Okasha

PHILOSOPHY OF LAW Raymond Wacks

PHILOSOPHY OF MIND Barbara Gail Montero

PHILOSOPHY OF PHYSICS David Wallace

PHILOSOPHY OF SCIENCE Samir Okasha

PHILOSOPHY OF RELIGION Tim Bayne

PHOTOGRAPHY Steve Edwards

PHYSICAL CHEMISTRY Peter Atkins

PHYSICS Sidney Perkowitz

PILGRIMAGE Ian Reader

PLAGUE Paul Slack

PLANETARY SYSTEMS Raymond T. Pierrehumbert

PLANETS David A. Rothery

PLANTS Timothy Walker

PLATE TECTONICS Peter Molnar

PLATO Julia Annas

POETRY Bernard O’Donoghue

POLITICAL PHILOSOPHY David Miller

POLITICS Kenneth Minogue

POLYGAMY Sarah M. S. Pearsall

POPULISM Cas Mudde and Cristóbal Rovira Kaltwasser

POSTCOLONIALISM Robert Young

POSTMODERNISM Christopher Butler

POSTSTRUCTURALISM Catherine Belsey

POVERTY Philip N. Jefferson

PREHISTORY Chris Gosden

PRESOCRATIC PHILOSOPHY Catherine Osborne

PRIVACY Raymond Wacks

PROBABILITY John Haigh

PROGRESSIVISM Walter Nugent

PROHIBITION W. J. Rorabaugh

PROJECTS Andrew Davies

PROTESTANTISM Mark A. Noll

PSYCHIATRY Tom Burns

PSYCHOANALYSIS Daniel Pick

PSYCHOLOGY Gillian Butler and Freda McManus

PSYCHOLOGY OF MUSIC Elizabeth Hellmuth Margulis

PSYCHOPATHY Essi Viding

PSYCHOTHERAPY Tom Burns and Eva Burns-Lundgren

PUBLIC ADMINISTRATION Stella Z. Theodoulou and Ravi K. Roy

PUBLIC HEALTH Virginia Berridge

PURITANISM Francis J. Bremer

THE QUAKERS Pink Dandelion

QUANTUM THEORY John Polkinghorne

RACISM Ali Rattansi

RADIOACTIVITY Claudio Tuniz

RASTAFARI Ennis B. Edmonds

READING Belinda Jack

THE REAGAN REVOLUTION Gil Troy

REALITY Jan Westerhoff

RECONSTRUCTION Allen C. Guelzo

THE REFORMATION Peter Marshall

REFUGEES Gil Loescher

RELATIVITY Russell Stannard

RELIGION Thomas A. Tweed

RELIGION IN AMERICA Timothy Beal

THE RENAISSANCE Jerry Brotton

RENAISSANCE ART Geraldine A. Johnson

RENEWABLE ENERGY Nick Jelley

REPTILES T. S. Kemp

REVOLUTIONS Jack A. Goldstone

RHETORIC Richard Toye

RISK Baruch Fischhoff and John Kadvany

RITUAL Barry Stephenson

RIVERS Nick Middleton

ROBOTICS Alan Winfield

ROCKS Jan Zalasiewicz

ROMAN BRITAIN Peter Salway

THE ROMAN EMPIRE Christopher Kelly

THE ROMAN REPUBLIC David M. Gwynn

ROMANTICISM Michael Ferber

ROUSSEAU Robert Wokler

RUSSELL A. C. Grayling

THE RUSSIAN ECONOMY Richard Connolly

RUSSIAN HISTORY Geoffrey Hosking

RUSSIAN LITERATURE Catriona Kelly

THE RUSSIAN REVOLUTION S. A. Smith

SAINTS Simon Yarrow

SAMURAI Michael Wert

SAVANNAS Peter A. Furley

SCEPTICISM Duncan Pritchard

SCHIZOPHRENIA Chris Frith and Eve Johnstone

SCHOPENHAUER Christopher Janaway

SCIENCE AND RELIGION Thomas Dixon and Adam R. Shapiro

SCIENCE FICTION David Seed

THE SCIENTIFIC REVOLUTION Lawrence M. Principe

SCOTLAND Rab Houston

SECULARISM Andrew Copson

SEXUAL SELECTION Marlene Zuk and Leigh W. Simmons

SEXUALITY Véronique Mottier

WILLIAM SHAKESPEARE Stanley Wells

SHAKESPEARE’S COMEDIES Bart van Es

SHAKESPEARE’S SONNETS AND POEMS Jonathan F. S. Post

SHAKESPEARE’S TRAGEDIES Stanley Wells

GEORGE BERNARD SHAW Christopher Wixson

MARY SHELLEY Charlotte Gordon

THE SHORT STORY Andrew Kahn

SIKHISM Eleanor Nesbitt

SILENT FILM Donna Kornhaber

THE SILK ROAD James A. Millward

SLANG Jonathon Green

SLEEP Steven W. Lockley and Russell G. Foster

SMELL Matthew Cobb

ADAM SMITH Christopher J. Berry

SOCIAL AND CULTURAL ANTHROPOLOGY John Monaghan and Peter Just

SOCIAL PSYCHOLOGY Richard J. Crisp

SOCIAL WORK Sally Holland and Jonathan Scourfield

SOCIALISM Michael Newman

SOCIOLINGUISTICS John Edwards

SOCIOLOGY Steve Bruce

SOCRATES C. C. W. Taylor

SOFT MATTER Tom McLeish

SOUND Mike Goldsmith

SOUTHEAST ASIA James R. Rush

THE SOVIET UNION Stephen Lovell

THE SPANISH CIVIL WAR Helen Graham

SPANISH LITERATURE Jo Labanyi

THE SPARTANS Andrew Bayliss

SPINOZA Roger Scruton

SPIRITUALITY Philip Sheldrake

SPORT Mike Cronin

STARS Andrew King

STATISTICS David J. Hand

STEM CELLS Jonathan Slack

STOICISM Brad Inwood

STRUCTURAL ENGINEERING David Blockley

STUART BRITAIN John Morrill

THE SUN Philip Judge

SUPERCONDUCTIVITY Stephen Blundell

SUPERSTITION Stuart Vyse

SYMMETRY Ian Stewart

SYNAESTHESIA Julia Simner

SYNTHETIC BIOLOGY Jamie A. Davies

SYSTEMS BIOLOGY Eberhard O. Voit

TAXATION Stephen Smith

TEETH Peter S. Ungar

TELESCOPES Geoff Cottrell

TERRORISM Charles Townshend

THEATRE Marvin Carlson

THEOLOGY David F. Ford

THINKING AND REASONING Jonathan St B. T. Evans

THOUGHT Tim Bayne

TIBETAN BUDDHISM Matthew T. Kapstein

TIDES David George Bowers and Emyr Martyn Roberts

TIME Jenann Ismael

TOCQUEVILLE Harvey C. Mansfield

LEO TOLSTOY Liza Knapp

TOPOLOGY Richard Earl

TRAGEDY Adrian Poole

TRANSLATION Matthew Reynolds

THE TREATY OF VERSAILLES Michael S. Neiberg

TRIGONOMETRY Glen Van Brummelen

THE TROJAN WAR Eric H. Cline

TRUST Katherine Hawley

THE TUDORS John Guy

TWENTIETH‑CENTURY BRITAIN Kenneth O. Morgan

TYPOGRAPHY Paul Luna

THE UNITED NATIONS Jussi M. Hanhimäki

UNIVERSITIES AND COLLEGES David Palfreyman and Paul Temple

THE U.S. CIVIL WAR Louis P. Masur

THE U.S. CONGRESS Donald A. Ritchie

THE U.S. CONSTITUTION David J. Bodenhamer

THE U.S. SUPREME COURT Linda Greenhouse

UTILITARIANISM Katarzyna de Lazari-Radek and Peter Singer

UTOPIANISM Lyman Tower Sargent

VETERINARY SCIENCE James Yeates

THE VIKINGS Julian D. Richards

VIOLENCE Philip Dwyer

THE VIRGIN MARY Mary Joan Winn Leith

THE VIRTUES Craig A. Boyd and Kevin Timpe

VIRUSES Dorothy H. Crawford

VOLCANOES Michael J. Branney and Jan Zalasiewicz

VOLTAIRE Nicholas Cronk

WAR AND RELIGION Jolyon Mitchell and Joshua Rey

WAR AND TECHNOLOGY Alex Roland

WATER John Finney

WAVES Mike Goldsmith

WEATHER Storm Dunlop

THE WELFARE STATE David Garland

WITCHCRAFT Malcolm Gaskill

WITTGENSTEIN A. C. Grayling

WORK Stephen Fineman

WORLD MUSIC Philip Bohlman

THE WORLD TRADE ORGANIZATION Amrita Narlikar

WORLD WAR II Gerhard L. Weinberg

WRITING AND SCRIPT Andrew Robinson

ZIONISM Michael Stanislawski

ÉMILE ZOLA Brian Nelson

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HANNAH ARENDT Dana Villa

BACTERIA Sebastian Amyes

BUSINESS ETHICS Nils Ole Oermann

BRITISH CINEMA Charles Barr

THE NOVEL Robert Eaglestone

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Simon Leather

Insects

A Very Short Introduction

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Foreword

This is a special book, the culmination of Simon’s sixty-year passion for insects, both as a hobby and a profession. His aim was to bring the wonder of insects to a wider audience so he was delighted to have the opportunity to write this Very Short Introduction (VSI).

Simon spent his early life in the Tropics and fell in love with insects as a child in Jamaica; he wanted to find out how insects worked and how they behaved. He studied Agricultural Zoology at Leeds University, where he discovered a passion for aphids, then completed a PhD at the University of East Anglia (UEA), studying the ecology of the bird-cherry-oat aphid. Two short post-doctoral fellowships followed, one in Finland, developing a prediction system for the same aphid, another back at UEA.

For ten years, he worked for the Forestry Commission based in Roslin, Midlothian, researching and advising on forest pests, particularly the pine beauty moth and the large pine weevil, but he missed academia and was pleased to be appointed as a Lecturer at Imperial College London, based at the Silwood Park campus, where for twenty years he lectured and conducted research on agricultural, horticultural, and forest pests. He discovered the joy of urban ecology, researching the biodiversity of Bracknell’s infamous roundabouts, which later inspired the name of his blog (‘Don’t Forget the Roundabouts’).

In 2012, he was delighted to move with his team to Harper Adams University (HAU), where he was proud to be appointed as the first UK Professor of Entomology. He spent nine happy years at HAU, basking in the collegiality, interacting with colleagues from all disciplines, and, most particularly, with students; he just loved to share his passion, and to support and mentor the next generation of entomologists.

He realized that social media could enhance science communication by reaching a far wider audience, and joined the Twittersphere (@Entoprof), tweeting and retweeting all things entomological and ecological but also personal: his walks and footpaths that needed repair, the view from home, France (where he hoped to retire), Brexit, Covid, Sunday roasts, and much more. He built up a following of almost 10,000 people, many of whom knew him only virtually.

He also started a blog (‘Don’t Forget the Roundabouts’), posting at about ten-day intervals for the rest of his life, on a myriad subjects, often his beloved aphids but anything that piqued his interest: insect idioms (e.g. a gnat’s whisker), tidy desks (not his own!), the dearth of entomologists, insects in children’s literature, classical entomological equipment, family history, papers that influenced his thinking and books that he enjoyed, dead entomologists, ‘Insectageddon’, together with a regular Pick & Mix of links that he thought worth sharing. He wrote natural history haikus and illustrated some blogs with hand-drawn cartoons; indeed many of his blogs were mini papers, supported by data, graphs, figures, and references He expounded on institutional vertebratism, a term that he coined to describe the concentration of effort and funding towards conserving vertebrates, often furry animals, at the expense of vastly more numerous and more important invertebrates.

Had he not been an entomologist, Simon might have been a writer. He was a voracious reader, owning 10,000 books, all of which he had read, and writing generally came easily to him; he published well over 200 papers and wrote or edited a number of books. He served as an editor or editorial board member for various ecological journals over many years, and refereed countless papers. He founded the Leather Family History Society, to foster research into his family name, writing articles and books to document what he and others discovered.

Simon was convivial; he seemed to know everyone in the world of entomology. Wherever he worked, he engaged with colleagues, enjoying coffee-room chats. He loved meetings and conferences, getting together with colleagues who became friends, sharing meals and a beer or, preferably, glass of red wine. As a fellow ecologist said, ‘he was the first person to look for at conferences’. As part of his outreach, he developed a suite of entertaining talks to engage groups such as the University of the Third Age (U3A), gardening societies, and the Women’s Institute (WI). He contributed to summer schools, careers fairs, and initiatives such as Skype a Scientist to enthuse young people about insects. Simon was an Honorary Fellow of the Royal Entomological Society recognising his outstanding contributions to entomology.

In retirement, Simon planned to synthesize everything that he had learnt about insects and to share this knowledge as widely as possible. Sadly this book is his swansong; he died in September 2021, not long after the manuscript was accepted for publication. In his last blog post, he described the difficulty of writing this VSI as he found that he knew both too much and not enough about insects; but while it was frustrating, it was also one of his most satisfying pieces of writing. ‘I just hope that…my readers will find as much to enjoy as I have since I first came across insects just over sixty years ago.’ I hope so too.

Hugely grateful thanks to Professor Helen Roy MBE Hon. FRES, ecological entomologist at the UK Centre for Ecology & Hydrology, for stepping in to see this book through to publication.

Dr Gillian Leather

Preface

Insects are a wonderfully diverse group but they are all animals with an exoskeleton (a supporting skeleton on the outside) made of the protein chitin, a three-part body plan—head, thorax, abdomen, three pairs of jointed legs, compound eyes, and one pair of antennae. They probably comprise 75 per cent of all animal life.

They range in size from tiny parasitic wasps, Dicopomorpha echmepterygis, a mere 139 micrometre (μm) long, to the titan beetle (Titanus giganteus), which can reach 17.5 centimetres (cm). Insects are found on all continents and habitats, from the hottest deserts to the frozen Antarctic, in caves, in the soil, inside plants, in other insects and vertebrates, in watercourses and bodies of water, and in the watery interiors of pitcher plants. While no insects live beneath the waves, the intrepid sea skaters, bugs in the genus Halobates, skim the surface of some oceans.

Insects include predators, parasites, herbivores, detritivores, fungivores, and saproxylics, that live on decaying wood. Some are regarded as pests while others are valued as beneficial. Some live colonially in a highly complex caste system; others live solitary lives, mingling only to mate or overwinter. Some, such as the honey bee and the silk moth, have been domesticated for millennia; others are used for biological control and protect our crops. Many provide highly nutritious, healthy food sources for humans. Some are excellent vectors of plant and animal disease; others have been used in human medicine, for instance in maggot therapy, and in the treatment of children with mental health issues and adults suffering from forms of dementia. They have inspired artists, sculptors, poets, musicians, novelists, and engineers, and provide the shock element in many horror films. Their images have appeared on postage stamps and bank notes; their preserved forms, framed under glass, adorn many a household’s walls.

Their rigid exoskeleton and associated musculature endow insects with great strength relative to their size while their rapid reproductive rates and adaptability have allowed many species to evolve resistance to commonly used insecticides. Many species have an intimate and obligate relationship with symbiotic bacteria that allows them to use food sources, such as wood, phloem, and xylem sap, that other animals are unable to exploit.

Their nervous system may be simple compared with that of mammals but they exhibit parental care, respond to complex visual and olfactory signals, migrate thousands of miles, ‘feel’ or at least react to pain, and learn from experience.

Many are masters of disguise, mimicking more well-defended species. Others sequester toxic chemicals from their host plants to protect themselves against predators while yet others disguise themselves as living or dead plant parts or blend so well into the background that it is only when they move that they reveal their true nature.

New species are described every day and many more await discovery, even in well-studied parts of the world. Climate change and habitat degradation threaten the existence of tens of thousands of species, the consequences of which will almost certainly be detrimental to ecosystems worldwide. We know much about insects, and yet there is also much we do not know.

Although there are only approximately 5,500 species of mammals, the mammal-biased perception of the animal kingdom has led to imbalances in funding and research at the expense of other more speciose vertebrate groups, such as the reptiles—c.10,000 species—and fish—over 30,000 species. This is, however, dwarfed by the dearth of funding and the paucity of researchers devoted to the study of insects (entomology) and other invertebrates. More than a million insect species have been described, with probably at least another five to eight million species waiting to be named. Given the diversity, utility, and beauty of the insect world, this is a calamity. Insects are the bedrock on which human civilization rests; without them there would almost certainly be no humans.

In the words of W. C. Allee (1938) in his excellent book The Social Life of Animals, ‘A survey such as I am attempting here should not try to be exhaustive’. I have taken his words to heart; entomology is a vast subject, and I have had to omit a great deal. I have based this book on the facts about insects that I have taught to students over the past thirty years, with the aim of telling a story that conveys the wonder and awe that insects have inspired in me. I hope that you, the reader, will share my feelings of excitement about these wondrous animals.

Acknowledgements

First, a huge thank you to my wife Dr Gillian Leather, who has put up with my entomological ramblings for more than thirty years and has played the part of the educated layperson in reading, re-reading, and stripping away the more verbose and prolix of my sentences. I am extremely grateful to Dr Christine Pearson of the Open University for her comments from the viewpoint of a botanist and communicator to students with many and varied backgrounds. I am also indebted to my former colleague Dr Patricia Reader for her very helpful entomological comments and insights. Dr Simon Segar generously provided the phylogenetic trees. I am deeply grateful to Latha Menon of OUP for her generous and incisive final edit of the completed manuscript. Finally, my heartfelt thanks to the hundreds of students I have taught over the years, who have allowed me to express my love of entomology in a relatively jargon-free manner.

List of illustrations

1 The appearance of insects through the ages and their evolutionary relationships
Modified after Mishof et al. (2014)

2 Basic body plan of an insect
Universal Images Group North America LLC / Alamy Stock Photo (from: http://www.earthlife.net/insects/anatomy)

3 A selection of insect wings showing the wide variation in venation
Images sourced from Simon Shim/Shutterstock, Mick Talbot/Flickr, Tunart/iStock, Scott Bauer, and Sharon Rogers

4 The central nervous systems of various insects
From The Insects: An Outline of Entomology by P. J. Gullan

5 Fourth-instar alatiform aphid nymph

6 Simplified phylogenetic tree of the insects, focusing on the Polyneoptera
Tree modified after Wipfler et al. (2019)

7 Thrips wing
Mound LA, Collins DW, Hastings A (2018). Thysanoptera Britannica et Hibernica—Thrips of the British Isles. Lucidcentral.org, Identic Pty Ltd, Queensland, Australia

8 Generalized female and male reproductive systems

9 Typical insect reproductive pattern

10 The ‘phenological window’

11 A termite mound
Adam Seward/Alamy Stock Photo

12 Termite and ant castes
From Encyclopædia Britannica, Inc., and Sakurra/Shutterstock

13 Japanese fighting aphids
After T. G. Whitham (1979) and S. Makino (1982)

14 Three aphid trophobiotic organs

15 Green island leaf-mine of the moth Stigmella atricapitella
Photo: Mike Shurmer

16 Influence of Wolbachia on green island formation
© 2010 The Royal Society

17 Generalized lifecycle of a mayfly

18 Larval and adult forms of the Plecoptera

19 Larval stages of a dragonfly
Goran Safarek/Shutterstock

20 Caddisfly fishing net
Photo: Jan Hamrsky

21 Batesian and non-Batesian mimicry
From Henry Walter Bates (1862)

22 Müllerian mimicry in butterflies
© 2006 Axel Meyer

23 Adult Uropyia meticulodina masquerading as a dead leaf
Photo: LiCheng Shih/Flickr

24 The map butterfly, the plant that is the mimic model for the eggs and the eggs of the butterfly.
From Jörg Hempel, and Sabine Zierer from Pixabay Source: Wikimedia File:Bee March 2008-2.jpg - Wikimedia Commons

25 Gastropacha quercifolia eggs
Photo: Hsuepfle/Wikimedia Commons

26 The darkling beetle

27 Difference in herbivore load between the simple plots and the weedy rows
© 1973 by the Ecological Society of America

28 Cropping systems: (a) Conventional intensive agricultural landscape; (b) the intercrop melange effect

29 Biological control in theory

30 The bee orchid with pollinator
Photos: The Orchids of Britain and Europe Source: Wikimedia File:Araschnia levana eggs.jpg - Wikimedia Commons

31 Changes in abundance of three common insect species

List of tables

1 The Apterygota

2 The Exopterygota

3 The Endopterygota

4 The relative toughness of plants

Chapter 1

In the beginning

Arthropods are, with good cause, often described as the most diverse and successful group of animals in the world. As well as insects, they include spiders, millipedes, scorpions, shrimps, crabs, woodlice, and, perhaps surprisingly to many, the barnacles. The word arthropod is derived from the term arthropodization—hardened (sclerotized) appendages with rings of soft unsclerotized cuticle in between, in contrast to animals with soft cuticles. The word ‘arthropod’ can be translated as jointed foot. Arthropods are also characterized by tagmata, functionally and structurally distinct batches of segments; in the case of the hexapoda, there are three—head, thorax, and abdomen. The body of an arthropod is covered by a chitinous exoskeleton to which the body parts and muscles are attached internally. Arthropods shed their exoskeletons to grow, a process known as moulting. After moulting, the arthropod expands its body by swallowing or taking in air to fill the new skeleton before it hardens. Once the adult stage is reached, moulting stops and there is no further growth. Their success can be attributed to their very adaptable body plan. The evolution of many types of appendage—antennae, claws, wings, and mouthparts—has allowed arthropods to occupy nearly every niche and habitat on earth.

Animal life began in the oceans and remained there for hundreds of millions of years until, about 500 million years ago (MYA), an arthropod left the water to live on land. This was the first of many; fossil evidence shows that arthropods invaded the land several times, and that different groups, including the ancestors of the first insects and their closest relatives, the Entognatha, made the ocean-to-land transition at different times.

Within the phylum Arthropoda sits an extremely speciose and successful group of organisms: the class Insecta. Insects are six-legged organisms, or hexapods, and are further nested within the Pancrustacea alongside the non-hexapod arthropods like crabs and shrimps, possessing as they do chitinous exoskeletons and jointed appendages. The word insect is derived from the Latin insectum—notched or divided body. The class Insecta is well defined; all living insects arose from a common ancestor which was a six-legged creature with a three-segmented body, jointed legs, and a single pair of antennae. These antennae helped the early land colonists to navigate around their new environment using chemical cues. The ancestors of insects were probably cave dwelling crustacea, the Remipedia, and as they diversified, several groups emerged around 479 MYA. The non-insect hexapods (the coneheads, springtails, and two-pronged bristletails) can often be found in damp habitats like soil, whereas the earliest true insects (the jumping bristletails and silverfish) were already more adventurous by the time they appeared on the scene around 440 MYA. Two pairs of wings opened up a three-dimensional world as insects took to the air 406 MYA. Some of the descendants of these first winged insects (the dragonflies, damselflies, and mayflies) still return to the water for breeding, but, in the case of dragonflies and damselflies, they dominate local airspace as voracious predators. From then on there was relentless diversification and constant adaptation, as they tracked the evolution of flowering plants. Other advances, for example, transitioning from continuous development to a lifecycle involving a pupal stage, allowed insects to reorganize their cells so that the adult insect was barely recognizable when compared with the larval form. This remarkable ability was something that confused many of the early entomologists who often mistakenly described larval and adult forms as different species. The evolution of sociality (Chapter 4) allowed some insects to develop complex societies involving a redistribution of roles within the colony. Throughout their tenure on land, insects have been masters at interacting with other organisms and are found both consuming and pollinating plants, gaining sustenance as detritivores, carnivores, or even feeding off the living tissue of their prey. Their myriad adaptations and tight integration with other life on Earth have been key determinants of their success.

Bernhard Misof from Zoologisches Forschungsmuseum, Alexander Koenig based in Bonn, and a host of colleagues from around the world, recently produced an extremely detailed classification of insects, based on genetics combined with an analysis of fossil records. The phylogenetic trees (showing the relationships between organisms based on comparison of their DNA) that they produced are far too complicated for this book, but are summarized simply in Figure 1 and the accompanying text. To reiterate, insects are six-legged arthropods which are now grouped as members of the subphylum Hexapoda, which includes the Collembola, Protura, and Diplura, now all placed within the class Entognatha, in reference to the fact that their mouthparts, unlike those of insects, are retracted within the head.

1. The appearance of insects through the ages and their evolutionary relationships.

The position of insects within the animal kingdom

Kingdom | Animalia
Phylum | Arthropoda
Clade | Pancrustacea
Subphylum | Hexapoda
Class | Insecta

Linnaeus (1758).

The insects, which greatly outnumber the Entognatha, are grouped in the class Insecta and are ectognathous: their mouthparts are exposed. Despite their superficial resemblance to arachnids such as spiders, the nearest relatives to the Hexapoda are the crustaceans, from which they diverged sometime in the middle of the Ordovician Period, some 460 MYA.

Insects have lived on Earth for almost 500 million years (Figure 1), possibly even longer, as recent discoveries suggest that they arose in the Ordovician Period and were well established by the Silurian, which began some 440 MYA. Fossil insects in amber from the Cretaceous Period (145‒66 MYA) are very common, but many insect fossils are also found in shale deposits from the mid-Triassic (around 220 MYA) as well as the Silurian.

Based on the structure and function of their respiratory system, which is based on an air-exchange system (see below), and the fossil record, it was assumed that the first insects were terrestrial. Extensive molecular genetic analysis has confirmed this, and it is now accepted that insects arose from cave dwelling crustacea derived from an earlier aquatic crustacean ancestor. Modern aquatic insects represent those that have returned to their ancestral habitat. Perhaps counterintuitively to us as relatively large mammals, the small size of insects is one of the reasons for their success. Most insects have a body size from 1 to 10 millimetres (mm), allowing them to exploit many habitats that would otherwise be inaccessible; some leaf-miners can complete their whole development within a single leaf. The evolution of flight, their diversity of feeding habits, and their flexible lifecycles allowed insects to conquer first the land and then the air.

Structure and function

The head of insects, even in the apparently soft-bodied orders, is heavily sclerotized. The thorax is divided into three segments, the pro-, meso-, and metathorax, and the abdomen can have up to twelve segments. Not all insects have wings and legs; larval stages never have wings and some, depending on where they live, also lack legs. But where present, legs and wings arise from the thorax, with one pair of legs on each segment; in the case of winged insects, the forewings arise from the metathorax and the hind wings from the mesothorax (Figure 2).

2. Basic body plan of an insect: anatomy of a worker honeybee.

The outer skeleton, the cuticle, has two layers: the epicuticle, a thin, waxy, water-resistant outer layer covering the lower, much thicker, chitinous layer, the procuticle. This, in turn, is formed of two layers, the outer exocuticle and the inner endocuticle. The tough, but flexible endocuticle is formed of several layers of fibrous chitin and other proteins. The exocuticle, also made of chitin, is rigid and hardened (sclerotized), although in many soft-bodied insects it is much thinner, especially in the larval stages.

Insects are the only invertebrates that have developed the ability to fly. Wings, formed of outgrowths of the exoskeleton, are a feature of adult insects. The wings are strengthened by struts—veins—that divide them into segments—cells. Wing venation in insects ranges from the multi-celled, multi-veined complexity of the lacewings to the simplified yet extremely efficient wing of the housefly (Figure 3). Each cell and vein has a unique designation, enabling the taxonomist to distinguish among species and orders.

3. A selection of insect wings showing the wide variation in venation.

Ancestrally, insects have two pairs of wings but some have reduced the size of their hind or forewings, as in the Diptera (flies) and Stresiptera, to such an extent that they are no longer functional for flight but are used in a manner akin to a gyroscope. Some insects, such as the vine weevil (Otiorhynchus sulcatus), have lost the ability to fly altogether; others, including aphids, only have wings at certain stages of their lifecycle.

Insects do not have lungs; their respiratory system is based on a network of tubes called tracheae, analogous to the inner structure of the vertebrate lung. The tracheal system opens to the atmosphere through a series of thoracic and abdominal pores, spiracles, often visible to the naked eye. The insect can control the aperture of the spiracles in response to environmental conditions and some can close them completely to prevent the entry of parasitic nematode worms. The tracheae branch into smaller and smaller tubes—the tracheoles—as they pervade the insect body, delivering oxygen to the various organs, in some cases almost directly to the mitochondria, the structures within cells that provide them with their energy.

Although giant insects are often featured in horror stories and films—and, in the past, some insects were indeed much larger than those that we encounter today—insects are limited in size because of the way in which they breathe. Lacking lungs, they depend on the diffusion of oxygen across the thin skin of the tracheoles. Larger insects ventilate their tracheal system by muscular pumping of the body walls but even this does not compensate for the lack of lungs. The exoskeleton also brings with it some disadvantages, in that the surface:weight ratio means that the integument—the insect’s covering—becomes disproportionately heavy and susceptible to water loss. Giant arthropods are found only in water, although, somewhat perversely, the largest insects are land living.

Unlike us, insects do not have veins and arteries or a single circulatory pump. Instead, a system of muscular pumps moves the haemolymph, a watery fluid, usually colourless, but it can be yellow, green, blue, and sometimes red, through the body compartments. The main pump is, somewhat cumbersomely, called the pulsatile dorsal vessel, the back part of which is sometimes referred to as the heart, and the front, the aorta. We humans do love to anthropomorphize. In a similar way, we can think of the haemolymph as a rough equivalent to the blood of vertebrates. The haemolymph bathes the organs and mediates all chemical exchanges between tissues. The haemolymph is responsible for the transmission of hormones, the distribution of nutrients, and movement of waste products to the excretory organs. Unlike human blood, the haemolymph rarely contains respiratory pigments but in some groups, for instance the Plecoptera, haemocyanin (an ancestral method for oxygen transport) is sometimes present. The haemolymph also carries the haemocytes, the blood cells, which, in a similar way to our red and white blood cells, are responsible for defence against diseases, ‘blood clotting’, and nutrient storage and distribution.

The structure of the insect nervous system varies among orders (Figure 4) but is, as with us, based around a central nervous system. In all insects, the nerve cells, as with other animals, are contained in structures known as ganglia and those of all the head segments are fused to form the brain. In insects, in contrast to us, where it runs along our spine (dorsally), the main nerve cord runs along the underside of the body (ventrally), connecting the thoracic and abdominal ganglia. The insect brain is divided into three parts—the protocerebrum, which is associated with the eyes and contains the optic lobes; the deutocerebrum, which controls the antennae; and the tritocerebrum, which coordinates signals arriving from the body. Insects have three types of neuron: sensory neurons, which receive stimuli from the environment and transmit them to the central nervous system; interneurons, which are responsible for between-neuron communications; and motor neurons, which receive information from the interneurons and transmit information to the muscles and the hormone-producing neuroendocrine cells.

4. The central nervous systems of various insects showing the diversity of ganglia in the ventral nerve cord.

Insect sensory organs include the eyes, the antennae, and the feet. Most insects have two compound eyes; they may also have two or three simple eyes—ocelli. The compound eyes are composed of many single photoreceptors—ommatidia—which, although not very good for image resolution, are extremely good at detecting movement; think how difficult it is to sneak up on a housefly. The ocelli have better image resolution and have a major role in helping flying insects to keep on course when airborne. The antennae are an important part of an insect’s sensory repertoire and may have more than one sensory function—able to detect touch, movement, and chemicals, including pheromones. The ability of insects to detect pheromones is amazing: some insects can detect and respond to a few hundred molecules of pheromone in a cubic centimetre of air from a distance of 30 kilometres or so. In some insects there is a trade-off between vision and smell (olfaction); insects with large eyes tend to have smaller antennae. Other insects, cave-dwellers for example, are blind, and rely entirely on their antennae and touch receptors to know where they are. Insects also have sensory organs on their feet, with which they can detect texture and ‘flavour’.

Insect growth and development is known as metamorphosis, and is under the control of hormones delivered via the endocrine system. There are three types of hormone, the ecdysteroids (ecdysone is the most common), juvenile hormones, and neurohormones (neuropeptides), which can be regarded as messengers. Most of the hormones are produced by specialist neurosecretory cells. The corpora cardiaca, a pair of neuroglandular organs either side of the aorta and behind the brain, store and release hormones as well as making their own. The prothoracic glands secrete ecdysteroid, and the corpora allata secrete juvenile hormone. These two hormones are integral to the moulting and reproductive processes of all insects. The role and source of juvenile hormone involved in moulting were determined by a series of elegant, if somewhat gruesome, experiments by the insect physiologist Sir Vincent Wigglesworth in the late 1930s. These involved the decapitation of adult and immature individuals of the kissing bug (Rhodnius prolixus), the bodies of which were then attached to whole individuals, resulting in changes in the moulting process. He graphically demonstrated the inhibitory effect of juvenile hormone on the moulting process by writing his initials, using juvenile hormone and applying it directly to the cuticle of pre-adult individuals with a fine paintbrush. After the next moult his initials were clearly visible as unmoulted regions on the otherwise adult insect. Juvenile hormone is present in all insect orders irrespective of their lifecycle type. Nowadays molecular techniques allow us to investigate insect hormones in a more detailed, if less dramatic manner.

The more primitive—or as taxonomists term them, less derived—insects have an ametabolous lifecycle, which does not involve metamorphosis. Once hatched, they are miniature versions of the adult, lacking only genitalia; each moult signals a change in size, without a marked change in form. Other insects, such as grasshoppers, have a hemimetabolous lifecycle, with three distinct forms—egg, larval, and adult; the later stages of the larval form gradually take on adult attributes—a process known as incomplete metamorphosis. The final type of lifecycle, holometabolism, or complete metamorphosis, is exemplified by the Lepidoptera (butterflies and moths), in which there is a pupal stage between the larval and adult forms, during which a complete transformation of body structure occurs; this allows the insect to exploit different food sources during its lifecycle. The larger the insect, the longer it takes to moult and for the new exoskeleton to harden, thus exposing the insect to a longer period of vulnerability.

How many insects are there?

Given the recent concern about declines in insect numbers (see Chapter 9), it is important that we know how many insects there are globally. The figures given for each order in the following tables add up to just over a million described species. This is, however, only the tip of the iceberg. Insects are extremely diverse, incredibly numerous, and woefully understudied. Estimating how many species of insects there are is thus an extremely difficult task and has exercised the ingenuity of entomologists for some time. Perhaps the most controversial figure is that arrived at by the American entomologist Terry Erwin. Terry sampled trees in Panamanian forests in the early 1980s and estimated that there could be as many as thirty million insect species worldwide. Due to his many, somewhat contentious, assumptions, this figure is almost certainly an overestimate; the common consensus is five to eight million species, of which approximately 1.2 million have been named and described. Even if we accept the more cautious lower estimate, given that the rate of description is approximately 10,000 species per year, it will be at least another 400 years before all have been named and described, and of course we have to find them first.

Putting things in order

There are currently twenty-nine insect orders; there were thirty recognized orders when I started writing this book, but a detailed phylogenetic study by Eirik Tielka and colleagues at the University of Bristol, UK, suggests that Siphonaptera (fleas) should now be placed within the Mecoptera. Over the past few decades, molecular biology has resulted in some major reclassification, with some orders being combined and others raised, so it is possible that by the time you read this the number of orders will have changed yet again.

Insects, based on their type of metamorphosis, are divided into three super-orders, the Apterygota, the Endopterygota, and the Exopterygota. The Apterygota (Table 1), which includes bristletails and silverfish, are ametabolous; the Exopterygota (Table 2), hemimetabolous; and the Endopterygota (Table 3), holometabolous.

Table 1 The Apterygota

Protura | Coneheads
Diplura | Two pronged bristletails
Archaeognatha | Bristletails
Zygentoma | Silverfish

Table 2 The Exopterygota

Ephemeroptera
Mayflies (the name referring to the fact that the adults only live or are only winged for a day) are the oldest extant group with wings. They are also a bit of an oddity: unlike other Exopterygota, they have a winged subadult stage. They are a relatively small order with approximately 2,500 species worldwide. The Ephemeroptera along with the Odonata are the oldest winged insect groups, the Palaeoptera, arising about 350 MYA.

Odonata
Dragonflies and damselflies (their name is derived from the Greek for tooth, δόντι; despite their amazing flight capability, the name refers to their toothed mandibles). The wings get a mention when we get down to infra-orders: the dragonflies, Anisoptera, which are uneven; and the damselflies, Zygoptera, which are even. There are just over 6,300 species listed by the World Odonata List (https://www2.pugetsound.edu/academics/academic-resources/slater-museum/biodiversity-resources/dragonflies/world-odonata-list2/).

Dermaptera
Earwigs—leathery/skin/hide, referring to the forewings, which are also reduced in size. Despite this, the much larger, membranous hind wings are safely folded away beneath them. This is one of the smaller orders with about 2,000 described species.

Plecoptera
Stoneflies—wickerwork wings. About 4,000 species. Fossil stoneflies date back to the early Permian. Their larvae are aquatic.

Orthoptera
Grasshoppers and crickets—straight wings. As of February 2021, the Orthoptera species list puts the number of species at 28,869 http://orthoptera.speciesfile.org/HomePage/Orthoptera/HomePage.aspx

Dictyoptera
(also known as the Blattodea)

Cockroaches, termites, and allies—net wings. There are around 6,800 species in this order, most of which are found in the warmer parts of the world.

Notoptera
Ice crawlers (Grylloblattodea) and gladiators (Mantophasmatodea). Despite being wingless, ‘Notoptera’ translates as back wings; the name was coined when only extinct, winged, members of this order were known. This is a tiny order with only sixty species known.

Mantodea
Mantids (e.g. the very familiar the praying mantis—prophet or soothsayer). There are about 2,300 species of mantids, all of which are predators, both as juveniles and adults.

Phasmotodea
Phasmids, the stick insects, and leaf insects; phasma translates as apparition or ghost and presumably relates to their ability to blend into the background. There are about 3,000 species of stick and leaf insects, most of which are found in the tropics. Many are parthenogenetic.

Psocoptera
Bark and book lice—the name translates as gnawed or biting with wings. In this case the adjective refers not to the appearance of their wings but to the fact that the insects can bite. They are also able to take up water directly from the atmosphere so that they can exploit extremely dry environments. About 5,500 species have been described so far, and most of these in the last few years.

Embioptera
Web spinners—lively wings. Each species has a characteristic way in which they spin their webs. Entomologist Janice Edgerly-Rooks at Santa Clara University, USA, collaborated with musicians assigning musical notes to each limb movement to produce a music video of embiopteran silk spinning. This is another small order with only 200 species described to date.

Zoraptera
The opposite of the Notoptera, the angel insects, Zora meaning pure in the sense of not having any wings; unfortunately for the taxonomists who named this order, winged forms have now been found. This is the smallest order, with only thirty species.

Thysanoptera
Thrips (both the plural and singular)—thysan means tassel wings, although feather might be a more appropriate description. There are just over 6,000 species of thrips, a number of which are important pollinators, but it also includes some very important pest species.

Hemiptera
True bugs—this distinction is made because many people, especially in the USA, call all insects bugs. The name Hemiptera translates as half wings. The two former official suborders (Homoptera and Heteroptera) were very useful descriptions. The Homoptera includes aphids, in which both membranous wings, fore and hind, are similar to one another. The Homoptera are now referred to as the Sternorrhyncha and Auchenorrhyncha, reflecting the position of the mouthparts, which in the former are positioned between the front legs and the chest, and in the latter arise from the back of the head in the neck region. The Heteroptera such as Lygaeids (e.g. chinch bugs, which are often mistaken for beetles) retain the existing name. Hetero (i.e. different) refers to the fact that the forewings are hardened and often brightly coloured in comparison with the membranous hindwings. About 80,000 species have been described.

Phthiraptera
Lice—wingless louse. There are just under 5,000 species in this order of highly specialized insects, three of which have evolved to exploit different sites on the human body.

Table 3 The Endopterygota

Rhapidioptera
Snakeflies—needle, in this case referring to the ovipositor (egg-laying tube), not to the wings, which are similar to those of dragonflies. They belong to the Neuroptertida, three closely related orders, which includes the Megaloptera and the Neuroptera. This is one of the smaller insect orders with only 206 species.

Megaloptera
Alderflies, dobsonflies—translates as large wings. There are only about 300 known species, the immature stages of which are aquatic.

Neuroptera
Lacewings—translates as veined wings. This is the largest order within the Neuropterida, with just over 6,000 described. The larvae of many species are voracious predators and some are reared commercially for use as biological control agents.

Coleoptera
Beetles—translates as sheathed wings, referring to the hardened forewings, the elytra, that cover the membranous hind wings. The complex process of unfolding and refolding their hind wings means that many beetles are ‘reluctant’ to fly unless they really need to. Currently this is the order with the most (approximately 300,000) species described.

Strepsiptera
(sometimes referred to as Stylops)

Endoparasites of other insects. The name translates as twisted wings. Like flies, they have only two pairs of functional wings, the other pair having been modified into halteres. Unlike flies, their halteres are modified forewings. They are a very strange group of insects and their relationship to other insect orders is still unclear. They are rarely seen by entomologists which may explain why only 600 species have been described. They feature on the logo of the Royal Entomological Society.

Mecoptera
Scorpionflies, hanging flies—translates as long wings. Not all Mecoptera are winged but the winged flies do indeed have long wings in relation to their body size. There were, until they were joined by the fleas, only about 600 species worldwide.

Siphonaptera
Fleas—translates as tube, no wings; the tube part of the name refers to their mouthparts. Now regarded as being within the Mecoptera. Some 2,600 species of flea have been described to date and have really swelled the ranks of the Mecoptera.

Diptera
Flies—translates as two wings; the hind pair is reduced to form the halteres, which are a highly complex orientation and balancing device, sometimes compared with a gyroscope. This represents one of the largest orders with approximately 160,000 species described to date.

Trichoptera
Caddisflies, which are, evolutionarily speaking, closely related to the Lepidoptera. Instead of scales, however, they have hairy wings; at first glance, some species can be mistaken for small moths. There are about 14,500 species of Trichoptera.

Lepidoptera
Moths and butterflies—translates as scaly wings. The scales and how they interact with light are what gives many moths and butterflies their iridescent colours. There are at least 200,000 species of Lepidoptera. The Lepidoptera, Trichoptera, Mecoptera, and Diptera had a common ancestor about 300 MYA and are collectively known as the Panorpid complex.

Hymenoptera
Wasps, bees, ants—translates as membrane wings. Alternatively, and with thanks to Canadian entomologist Stephen Heard, Hymenaeus was the Greek god of marriage; Hymenoptera as ‘marriage wings’ makes sense because of the hamage wing coupling (fore- and hind wings coupled by a row of hooks, or hamuli, so that they beat as one wing). The Hymenoptera contain the Parasitica, wasps that have larval stages that develop within other insects; they almost certainly inspired the film Alien. Although 150,000 species have so far been described this is probably only the tip of the iceberg.

First, a little bit of entomological jargon; broadly speaking we are talking bastardized Greek and Latin. Pteron is Greek for wing and is the root of the Latin ptera, which occurs commonly in entomology. The presence of wings is denoted by the suffix ptera, the absence of wings by aptera, which can be a little confusing and, to further complicate matters, as in pterodactyl, the p in Apterygota, Endopterygota, and Exopterygota is silent.

In entomology, when we talk about wingless insects, we use the term apterous. Most insects, the Exopterygota and the Endopterygota, are winged. The Exopterygota are insects whose wings develop outside the body and show a gradual change from immature to adult. Think of an aphid for example; when the nymph (immature hemimetabolous insect) reaches the third or fourth instar (moulted stage), it seems to have shoulder pads; these are the wing buds (Figure 5). The process of going from egg to adult in this way is, as mentioned earlier, called incomplete metamorphosis.

5. Fourth-instar alatiform (destined to be winged) aphid nymph, showing the distinctive wing buds.

In insects such as butterflies and moths, where the wings develop inside the body, the adult bears no resemblance to the larva and the process is described as complete metamorphosis and the lifecycle type as holometabolous.

Now on to the orders and their names (Figure 6). Remember that aptera means no wings and ptera means with wings. This can be a bit confusing as most of the orders look and sound as though they have wings. This is in part, due to our pronunciation of words; we tend to make the syllables fit our normal speech patterns, so that words are not divided into their correct component parts. Diptera and Coleoptera are two good examples—we pronounce the former as ‘Dip-tera’ and informally as Dips but, from a purist’s point of view, it should be pronounced di-tera—two wings; similarly, coleo-tera, with a silent p.

6. Simplified phylogenetic tree of the insects, focusing on the Polyneoptera, which were the first orders to evolve the ability to flex their wings over their abdomens. The width of the black triangles indicates the number of described species within each order. The approximate dates of diversification are shown as millions of years ago.

Most of us, including entomologists, are most familiar with only seven of the insect orders, in order of species richness, the Coleoptera (beetles), the Hymenoptera (ants, bees, and wasps), the Diptera (flies), the Lepidoptera (moths and butterflies), the Hemiptera (true bugs), the Orthoptera (crickets and grasshoppers), and the Odonata (dragonflies and damselflies). Between them these orders account for about 900,000 species, so about 75 per cent of all those insects that have been described to date. Of these seven orders, the first five named actually account for just over 800,000 species. If we accept that the number of species within an order reflects their success, we might ask what it is that makes the Big Five so successful. One could argue that with the exception of the Lepidoptera, which are, with a handful of exceptions, all herbivorous, their success is because they, even the Hemiptera, range across the dietary spectrum, from scavengers through herbivores and omnivores to voracious predators, and are able to exploit a wide range of ecological niches. The Orthoptera on the other hand are wholly herbivorous and the Odonata largely carnivorous. That does not mean that the other orders are not important—they all have a part to play, and some of the smaller orders, such as the Thysanoptera (thrips (Figure 7) or thunderflies), include some of the world’s most important pests (Table 2). Other orders, such as the Zoraptera, are so small (sixty species) and so rare that only a handful of entomologists have ever seen them. Niche specialization does have some advantages, in that competition is reduced; the ice crawlers (Grylloblattodea), as their name suggests, live in icy caves and on frozen mountain tops, habitats where other insects are rarely, if ever, found. They are, however, extremely vulnerable to climate change and habitat loss, and are almost certainly the most endangered group of insects in the world.

7. Thrips wing, showing the characteristic feathery appearance.

There is some debate among entomologists as to which orders contain the most species. The beetles (Coleoptera), which have four wings, the forewings of which have become heavily sclerotized and cover the hind wings, to form ‘casings’ known as the elytra, have long been lauded as the most speciose insect order. The point was highlighted by the British evolutionary biologist and geneticist J. B. S. Haldane, who is purported to have told a group of theologians that if God existed he must have ‘an inordinate fondness for beetles’. Current estimates place beetles at the top of the podium with approximately 300,000 described species. However, based on an analysis using body size, collection rates, and the ratio of beetles to other insects housed in the Natural History Museum, London, Nigel Stork and colleagues suggest that there at least a million extant species of beetle. In second place are the Lepidoptera with 200,000, closely followed by the Hymenoptera with 150,000, and the Diptera at 120,000—although Erica McAlister, author of The Secret Life of Flies, puts the number at 160,000, with at least that many waiting to be discovered and named. Hymenopterists argue that as the Hymenoptera contain the Parasitica (wasps that parasitize other insects), and as all insects have parasites, the majority of which are Hymenoptera, and many of which are species specific, it is logical to suppose that the Hymenoptera must be the biggest order; we must, however, wait for the taxonomists to confirm this.

Having covered the basics of insect taxonomy and evolution, and their basic biology, we can now move on to an exploration of their behaviour and how this has enabled them to be so successful.

Chapter 2

Prolific procreators

Like other animals, the primary function of insects is to reproduce. All insects have the same basic reproductive structures (Figure 8). Females have a pair of ovaries, each of which is divided further into a series of tubes, containing rows of egg chambers, the ovarioles. The number of ovarioles varies between species, from as few as four per ovary in some aphids to more than fifteen in some species of flies. The more ovarioles, the more offspring an insect can produce. In some orders of insects, the number of ovarioles is a constant, most butterflies and moths, for example, have eight; in other groups, flies and aphids, the number of ovarioles varies both between and within species.

8. Generalized female and male reproductive systems.

Male insects produce sperm, which is delivered to the female via the penis, known as the aedeagus, although in some insects, such as bed bugs, the male can inject his sperm directly into the abdomen through the cuticle of the female, very appropriately termed traumatic insemination. Female genitalia vary among orders but in general there is an external opening connecting to the ovaries, and a sperm storage/receptacle (spermatheca). The sperm is often delivered in a ‘package’—the spermatophore, which, as well as holding the sperm, provides extra nutrients to the female—a type of nuptial gift (see p. 32). Most insects lay eggs, but some species, such as aphids, give birth to live young. Many insect species, such as vine weevils, some stick insects, and, most notably, aphids, are parthenogenetic, meaning they no longer require males to fertilize their eggs. Aphids are even more special in that each adult aphid contains live young, which in turn contain strings of embryos—a living Russian doll.

The number of offspring that a female insect produces is linked closely to her size; the larger the female, the more offspring she is able to produce. The size of an insect is largely the result of the quality of the nutrition that it receives as a larva; the better the larval diet, the larger the adult insect. As a consequence, finding the best place to deposit their young is very important for female insects, especially when the larvae have limited powers of dispersal. The optimal outcome would be for insect mothers to choose those hosts on which their offspring would prosper best and to lay as many eggs as possible on those hosts and this, with few exceptions, is generally what we see in nature. Herbivorous insects and those that parasitize other insects show great prowess in host selection (‘mother knows best’), choosing better quality hosts on/in which to lay (oviposit) their eggs. Predatory insects, like ladybird beetles and hoverflies, are also able to select egg-laying sites to optimize offspring survival; they lay their eggs near aphid colonies, ensuring a plentiful food supply in easy reach of their offspring when they emerge from their eggs. The offspring of herbivorous insects have been found to survive better on the host plants preferred by their mothers, and insects that are able to survive on a wide range of host plants are less ‘fussy’ than those with a more limited range of diets.

Fecundity, the number of offspring that an insect can produce, can be described as either potential—that which could be achieved under ideal conditions, or realized—or that which is actually achieved. An insect may have a potential fecundity of several hundred but lay only a handful of eggs, not all of which will hatch successfully. So-called capital breeders, normally those species which do not feed as adults, such as many of the Lepidoptera, use resources laid down during the larval phase, and no new eggs are developed as adults; whereas income breeders, mosquitoes for example, continue to obtain resources to develop and mature eggs, with new eggs being developed as adults. There is no evidence to suggest that income breeders are more fecund than capital breeders, although their response to adverse conditions may be more flexible.

Insects, even those that tend to live for a long time, are very vulnerable to predation and weather events, so it is important to lay as many eggs as possible as early as possible. Most insects produce the majority of their offspring in the first few days of adult life (Figure 9). In some species, over 50 per cent of eggs are laid in the first three or four days of reproductive life. Eggs laid subsequently are a bonus and some insects, if they survive, can continue to produce offspring for several weeks, or, in very long-lived insects, even months, although the offspring that arise from later-laid eggs are not as fit as those laid earlier; they tend to be smaller and the larvae that emerge are also smaller and have a lower chance of surviving to adulthood than their siblings from the earlier-laid eggs.

9. Typical insect reproductive pattern showing the number of offspring produced by a female insect once reproduction has begun.

Egg size can also vary according to the availability of suitable oviposition sites: the pine beauty moth (Panolis flammea), for example, will lay more and smaller eggs in the presence of good-quality host plants than if the available host plants are of poorer quality. On a good-quality host plant, the tiny larvae emerging from the small eggs can feed and survive with relative ease, whereas on a poorer quality host plant they need a better start in life and larger eggs are laid. Female insects will also delay oviposition if there is a lack of good-quality host plants, but given the vagaries of weather and the abundance of natural enemies, they are in a race against time to lay their eggs before they die. Stretch receptors in the abdomen tell them that they are full and eventually they will lay some eggs on a less suitable host to relieve the pressure. They then seek another host plant. If the next plant is of better quality, they will lay eggs on it; their expectations are then raised and they become choosier. However, if the next host plant is of poorer quality, they subsequently become less choosy. Of course, this pattern of oviposition depends on the overall egg-laying strategy of the species. Oviposition in insects, whether predatory, parasitic, or herbivorous, falls into three main categories—large clutches, small clutches, and singletons. There are arguments to be made in favour of all these strategies and no strategy is confined to any one order of insects. There are various reasons for the evolution of different clutch sizes among insects, ranging from reducing predation risk of the adults, and ensuring the safety of the larvae, to trade-offs between fecundity and dispersal.

Within the Lepidoptera, for example, oviposition strategies vary across families. Lepidoptera such as small ermine moths (Yponomeutidae), members of the Lasiocampidae, the eggars and lappet moths, and the Thaumetopoeidae, processionary moths, whose larvae live gregariously in silken webs or tents (hence their common names—tent caterpillars/tent moths), tend to lay their eggs in large masses, of up to 200 eggs. Other moths, such as the Lymantrinae, or tussock moths, whose females tend to be flightless or have reduced wings, also lay their eggs in large clusters, many covering their eggs with masses of spiny hairs broken off from their abdomens to protect them against predators. It is easy to see why insects whose ability to disperse is limited would lay all their eggs at once or in a few very large batches, but what about those where the females are relatively strong flyers? One argument is that large clusters of eggs reduce overall surface area and the risk of desiccation. If your eggs are toxic or protected with irritating hairs, it may make sense to advertise your presence and toxicity more visibly. Another factor that might encourage cluster laying is if the larvae are gregarious and egg hatch is well synchronized; hatch at the same time and, if there are a lot of you, the protective webbing can be fashioned more quickly. There is also some evidence that group feeding makes it easier to overcome plant defences whether you are a defoliator feeding on leaves or a bark beetle feeding underneath tree bark. Some cluster-laying insects, for example ladybirds, lay a number of eggs that are never destined to hatch but are there to provide the first meal for their larvae to build up their strength before they have to start hunting for prey. Finally, if your food source, be it aphids if you are a predator or plants if you are a herbivore, is distributed in a non-regular, patchy way, it makes biological sense for the mother insect to deposit a sizeable proportion of her offspring at a site where a plentiful supply of food is available.

Many insects have another strategy; they lay their eggs in singletons or pairs on the basis that it is faster to lay one egg at a time than to lay dozens or hundreds of eggs in one go. Less time is spent in one place, and the chance of being predated is reduced. If you have ever watched a cabbage white butterfly laying eggs, this is very obvious; each egg-laying event takes no more than a few seconds then the mother flits to another leaf. Insects adopting this strategy also tend to lay small, well-camouflaged—cryptic—eggs placed, if a plant feeder, on the underside of the leaf. This oviposition strategy relies on not being seen. Another advantage of cryptic, non-toxic eggs is that the larvae develop faster as they do not have to incorporate (sequester) poisons from their host plants as they grow. Finally, if there are only a few individual insects scattered across a whole plant, it makes the job of predators or other natural enemies more difficult, as they have to search harder, with fewer visual and chemical signals (in the form of leaf damage and volatile compounds) to inform them that a tasty meal is in the vicinity. Insects that lay more than one egg clutch, lay smaller clutches, containing smaller, less viable eggs, as they get older. The mortality of eggs laid by the rice stem borer, Chilo partellus, in the latter half of the mother’s life is twice that of eggs laid at the beginning of her reproductive life. Moreover, the larvae that do hatch from these late eggs have a much lower chance of surviving to become adults than their older siblings.

By the late 1970s, it was generally accepted that the optimal egg-laying strategy in herbivorous insects would be linked, first, to the number of eggs remaining in their ovaries; and, second, to the likelihood of encountering a suitable host plant on which to lay their eggs. In general, adult Lepidoptera are able to ‘remember’ host suitability for oviposition sites, altering their concept of a good-quality host depending on the suitability of the previous host plants that they encountered and the number of eggs left in their reproductive tract. Their degree of ‘fussiness’ thus waxes and wanes according to the suitability of the last host plant encountered, but this is tempered further by how long they have been on the hunt. As the reproductive clock ticks, the probability of them accepting a less suitable host on which to lay their eggs increases.

Similarly, we know that adult Lepidoptera, such as the monarch butterfly (Danaus plexippus), are able to retain learned information about suitable feeding resources, for example, the flowers that are likely to give them the most nectar. This ability is not just short-term: the hummingbird hawkmoth (Macroglossum stellatarum) is able to remember flower preferences even after winter dormancy.

Sexual selection and mating

Unless they are parthenogenetic, which many are, insects are sexually dimorphic, with the males and females of most insects differing in appearance. Insects have adopted a number of different strategies to locate mates, ranging from the use of sex pheromones to mass swarming and nuptial gifts, among which we can include the use of spermatophores, the casing produced inside the male containing sperm that is transferred during copulation.

In theory, female insects should choose males that will confer greatest fitness on their offspring. We would thus expect that male insects would evolve to display ever more extreme secondary sexual characteristics to satisfy the expectations of their potential mates. Although we can see some signs of this, for example the stalk-eyed flies, many insects instead show a great variation in their secondary sexual characteristics, with some male individuals investing less in display than others, yet still mating successfully.

Pheromones

Pheromones are semiochemicals, substances that elicit behavioural responses in another organism. Sex pheromones are used widely by insects: in some species females produce them to attract males, while in others males use them to attract females. Sex pheromones are usually very species specific, although in some closely related species the structure of the pheromones is identical but the concentrations at which they attract their respective recipients differ. Insects are able to detect pheromones from a considerable distance: some moths can respond to sex pheromones from as far away as 50 km. The highly specific blends of pheromones produced by insects ensures that the right mates find each other quickly and efficiently, increasing the chances of finding a mate even at low population densities. The downside for some of those insects that use pheromones to attract their mates is that chemists have been able to synthesize them and many are now used as a pest control method by attracting males into traps baited with pheromone lures.

Mating swarms, leks, displays, combative encounters

Many male insects find mates by aggregating to form swarms (referred to as leks), often of great size, that attract females and provide an opportunity for sexual competition, as the females, in theory, enter the swarm and pick the most robust and active males. This type of behaviour is termed lekking. Mayflies (Ephemeroptera) are renowned for the size and predictability of their short-lived but spectacular swarms. Ants, honeybees, some beetles, cockchafers, and many dipteran species, bibionids (march flies, known as love bugs in the USA), mosquitoes, and midges all have mating swarms. Midges tend to swarm on warm evenings, quite often at the top of a small hill or even above a human head. Within the male leks, theory has it that large insects are at an advantage over smaller members of the same species in many ways, including sexual competition. This is not always so: in the phantom midge (Chaoborus flavicans), while the large males form the lek, many of the smaller males rest on the vegetation and mate with females that have not yet entered the swarm. In a few species, the dance fly (Empis borealis) being a good example, the females form the swarm into which a single male enters, bearing a nuptial gift with which to entice a female to leave her sisters and join him in a mating flight.

Another group of flies, the stalk-eyed flies (Diopsidae), has evolved eyes that are borne on stalks, giving the appearance of a pair of antlers. This bizarre adaptation has two functions: mate attraction—females prefer males with longer eye stalks—and male competition. Males face each other and compare their relative eye spans. In some cases, they will spread their front legs apart to reinforce the message, the insect version of the power stance. If the relative eye span is similar, a fight will ensue, the winner holding the territory and gaining a suitably impressed mate.

Similar outsized modifications of body parts can be seen in male stag beetles (Lucanidae). The males have modified mandibles that resemble the antlers of stags, hence their common name. In the mating season, they use their antlers to wrestle other males, grabbing each other and using their antlers to overturn and throw each other to the ground. These fights can often be protracted and, as with stags, can result in physical injury to the loser.

Lepidoptera, in particular butterflies, adopt a strategy called ‘hill topping’: male swallowtails (Papilio machaon), for example, aggregate at the tops of hills and wait for females to fly up towards them. These hill-top sites are used year after year and are frequently visited by entomologists ‘in the know’. Butterflies can also be very territorial, some being perchers, others patrollers. Perching is a ‘sit-and-wait’ tactic; the males guard a territory, sometimes as large as 20 square metres (m²), in which they sit in a suitable, usually high position, from which they will emerge to investigate passing objects, either chasing away a competing male or attempting to mate with a receptive female. Patrollers, on the other hand, fly up and down a territory looking for receptive females with which to mate. Males of the North American great purple hairstreak butterfly (Atlides halesus) perch in the tops of trees waiting for receptive females but fly up from their perches to chase other males away from their territories, sometimes resorting to physical clashes as well as flight displays. The purple-edged copper butterfly (Lycaena hippothoe) is both a percher and a patroller. The aptly named speckled wood butterfly (Pararge aegeria) flies in partially shaded woodland with dappled sunlight. The males, which are very aggressive, usually perch in a small pool of sunlight, rising up to deter intruders; they will even attempt to chase humans away from their glades.

Nuptial gifts and spermatophores

Like some spiders, several male insects use nuptial gifts to help persuade their partners to pass their genes on. Probably the most well-known nuptial gift is that found in a few species of the praying mantis, in which the male risks his life while impregnating his chosen mate, especially if she is hungry. Death during copulation is not the male’s most favourable outcome: mating with more than one female allows a better chance of spreading his genes, although female mantids who eat their copulating partner can lay up to 30 per cent more eggs than those that allow the male to depart intact. Male scorpionflies (Panorpidae) have an array of tactics with which to attract mates. They use pheromones to attract potential mates but some species reinforce this with nuptial gifts: the male gives the female food, which she eats during copulation. The food item may be a salivary deposit from specially enlarged salivary glands or it may be a dead insect. The male waits for a female to arrive and copulates while she is busy with her meal. Some males dispense with both the gift and the pheromones and use their abdominal clamp to force the female to copulate with them; and in yet other species, the males mimic females and steal another male’s gift which they then proceed to use for their own benefit.

Perhaps a more intimate nuptial gift is the spermatophore. This may have been an adaptation to life on land, as the aquatic ancestors of insects may just have released sperm into the water; once on land, the sperm needed to be prevented from desiccating on its way to the female, especially in insects where the male does not introduce the sperm directly into the female. In some Orthoptera the males produce both a spermatophore and a nuptial gift (to stop her from eating the spermatophore before the sperm have entered her).

In the monarch butterfly, the larger the spermatophore, the longer the time before they mate again, which is an advantage to the first male on the scene; although females that mate more than once lay more eggs than single-mated females. Does it cost the males anything to be so generous? In some species (e.g. Tatochila mercedis sterodice) their lifespan is reduced, while in others, such as the speckled wood butterfly, there is no effect on lifespan. The spermatophore in Lepidoptera is an adaptation to the fact that in many insects, the last male to mate has more chance of fertilizing all the eggs. Preventing the already mated female from mating with another male by blocking her reproductive apparatus with a plug is thus a worthwhile investment. Other insect orders adopt similar tactics. In the cricket Gryllodes supplicans, the male attaches a large gelatinous mass (spermatophylax) to the smaller sperm package (ampulla). In this species as with other crickets, the spermatophore remains outside the body (although attached) and the female eats it. By having the attachment there is more chance of the sperm fertilizing the females, as the bigger the spermatophylax the longer it takes the female to reach the sperm parcel.

Clearly insects have a variety of means by which to pass on their genes, but to do this successfully they must also be able to move to new habitats and develop the adaptations needed to exploit them. Chapter 3 explores the ways in which insects have responded to this challenge.

Chapter 3

On the move

The insect wing is a remarkable structure. Aside from vertebrates, insects are the only animals that use flapping wings for locomotion, and winged insects make up 69 per cent of all animal species. Insects are unique among the invertebrates in that they have developed the ability to fly, although this characteristic has been lost in many species and some orders. Unlike those of other animals, insect wing muscles can contract multiple times for each single nerve impulse, allowing the wings to beat faster than would otherwise be possible. The muscles are attached longitudinally and vertically across the thorax to the exoskeletons, not directly to the bases of the wings; this is more efficient and allows more muscle connections. Dragonflies have additional small accessory flight muscles that control wing rotation while the larger muscles, which in other insects are used for both power and wing rotation, are used only for power.

The oldest winged insects, the Palaeoptera, are today only represented by the Odonata and Ephemeroptera; they differ from the other winged insects in that they are unable to fold their wings back over the abdomen. The Polyneoptera (Chapter 1, Figure 6) which arose about 350 MYA, are, like the other more recent insect groups, able to fold their wings back over their abdomens. It is thought that this modification evolved to protect their delicate wings from being damaged while moving through vegetation or confined spaces. In many insect groups the forewings are much thicker than hind wings and act as protective covers. The most extreme forms of this are seen in the Holometabola, especially within the Coleoptera, where the forewings are highly sclerotized into protective wing cases (elytra) and are no longer used for flight. Based on their wing structure, some members of the Polyneoptera were originally placed in the super order Orthopterida. Advances in molecular biology have, however, shown that this is not a valid classification, although the grasshoppers, crickets, and stick and leaf insects are still considered to be members of the Orthopterida.

Origin of insect flight

Insects are the only flying animals that have not sacrificed a pair of legs to gain the advantage of life in the air. They were the first animals to learn how to fly, at least 300 MYA. The first ‘fully fledged’ winged insect fossil record dates back 318 million years, to the late Carboniferous Period. Understanding how insect wings evolved has occupied the minds of entomologists for many years, and was made more difficult by the lack of what David Alexander, the world expert on animal flight, terms ‘informative fossils’. Two main theories, dating back to the latter part of the 19th century, dominated the field for more than a hundred years—the gill theory and the paranotal lobe theory.

The gill theory postulates that wings evolved from gills of aquatic larval insects. Modern aquatic insect larvae, such as mayflies, have external movable gills on the abdomen, which have air tubes arranged in branching patterns, looking very much like wings and their veins; against this theory is the fact that the gills are on the abdomen, and insect wings arise from the thorax. Proponents of the gill theory suggest that the ancestral forms also had gills on the thorax, although this does not explain why modern forms have lost them. Some modern insects use their abdominal gill plates to move, supporting the theory that the ‘lost’ thoracic gills were the precursors of wings. But against this argument is the fact that the tracheal system of insect respiration evolved on land and fossils show that the earliest insects were terrestrial with a fully developed tracheal system. Moreover, freshwater insects did not appear until the Triassic, 100 million years after terrestrial insects had appeared.

The paranotal lobe theory proposes that wings are derived from flat plates that evolved from the top of the thorax, perhaps originally as a side protection, camouflage, or extra anchoring for legs. As they increased in size they became used as devices for gliding or parachuting, and eventually became flexible enough to allow them to be used as steering devices. For this to work they needed a joint, which in turn needed muscles. As the proto-wings became larger and provided more lift, what began as weak steering movements evolved to powered flight. Against this theory, which has dominated the text books, is the fact that it requires evolution from scratch rather than selection from an existing structure.

Bounded ignorance

Frustrated by the lack of fossil evidence, some entomologists decided to approach the problem from another direction. In an influential review published in 1994, Joel Kingsolver and his colleague Mimi Koehl coined the phrase ‘bounded ignorance’. In essence this refers to the use of experiments and models to work out what is possible physically without knowing what the actual structure looks like. They made physical models based on reconstructions of fossil insects and came up with an alternative hypothesis: that wings arose from thoracic structures involved in maintaining core internal temperature (thermoregulation). When dislodged from their resting place on a tree, wingless ants and other arboreal non-winged insects are able to end up back on the tree more often than on the ground, despite having no specialized flight apparatus. This ‘directed aerial descent’, as it has been termed, turns out to be extremely common in non-winged arthropods; spiders, bristletails, silverfish, arboreal ants, and the non-winged nymphs of several insect species all do this to a greater or lesser degree. In light of this, Robert Dudley and Steve Yanoviak have proposed the following route to the evolution of flight:

Live on an elevated location, such as a tree → Be able to jump or fall in a controlled manner → Have the ability to flip back to front and/or land in a controlled manner → Develop the ability to parachute → Further development of directed aerial descent—body structures that are lift-based and drag-based to enable steep glide angles → Body structures enable gliding (predominantly lift-based, shallow glide angles) → Recognisable wing structures allowing sophisticated aerial manoeuvres → Flapping flight.

Until concrete fossil evidence is found, this sequence of events seems to be the most likely route to the evolution of flight in insects. A large number of species have now lost the ability to fly, which might seem strange given that the success of insects is attributed to being able to fly. Two contemporaries of Charles Darwin, Charles Lyell and Vernon Wollaston, both noticed that just over a third (36 per cent) of the beetles native to the island of Madeira were flightless. Darwin, who had been fascinated with beetles since his student days, hypothesized that on islands, natural selection would favour smaller, less flight-able beetles since larger beetles with bigger wings would have a greater chance of being blown out to sea and drowned. Their genes, unlike those of beetles living on the mainland, where being able to fly gave them an advantage over flightless individuals in locating food and mates, would then be lost to the island population. Although this is a compelling idea, it is not necessarily totally correct.

Almost a hundred years later, the American entomologist Philip Darlington, a specialist on carabid beetles, noted that many of the flightless beetles on Madeira were carabids, a family that is well-known for having a high proportion of wingless species. Carabids, many of which are voracious predators, have evolved three different lifestyles: those that live almost exclusively on the ground (geophiles), those that frequent stream and river banks (hydrophiles), and those that live in trees (arborophiles). The geophiles, living and foraging on the ground and rarely needing to fly, have, over millions of years, evolved into long-legged, short-winged, strong-jawed killing machines. A large proportion of the beetles living on Madeira were geophilous carabids, so Darwin was only partially right in his hypothesis of how natural selection on Madeira had produced so many flightless beetles. He was, of course, entirely correct in attributing the presence of so many flightless beetles to natural selection.

Migratory urge

We often hear about the remarkable migrations of butterflies such as the monarch and painted lady, whose annual multi-generational migrations extend over thousands of kilometres, flowing north and south, with the seasons, tracking changes in their food resources that follow a predictable climate-related pattern of spring flushes and summer declines. Similarly, the plagues of locusts and armyworms that spread out across large parts of Africa to devastate crops reflect the build-up of fast-breeding populations chasing fresh food resources. Long-distance travel is, however, not just confined to the larger insects. There is a common misperception that small insects, such as aphids, are no more than aerial plankton; this is not always the case. In 1924, Charles Elton, regarded as the founder of modern animal ecology, while on an expedition to the ice-covered island of Nordaustlandet, the second largest of the Spitsbergen group, reported finding large numbers of the greater black spruce aphid (Cinara piceae), many of which were still alive. Elton suggested that the aphids came from the Kola Peninsula, some 1,300 km away, carried by strong south and south-east winds. He estimated that they would have made the journey in twelve to twenty-four hours. This was regarded as an example of totally passive migration and was used as one of many examples of aerial plankton. This is probably not giving aphids credit for their ability to actively fly long distances. During the 1960s, Roy Taylor and colleagues from Rothamsted Research, UK, sampled aphids 610 m above the ground using aeroplanes, and concluded that although the aphids were using jet streams, they were flying rather than floating, and that they descended to the ground in the evening to rest for the night.

Aphids are remarkable for another facet of their migratory abilities. The ovarioles of aphids vary in number not only between but also within species. Even more remarkable is the fact that the offspring from a single clone mother—and remember, they too are clones—also vary in the number of ovarioles that they possess. In the winged forms (alate exules) produced on the secondary host plants of Rhopalosiphum padi, the number of ovarioles can range from four to ten. This variability of ovariole number in the dispersal morphs of aphids that spend much of their lifecycle on ephemeral host plants is quite common. So why do so many aphid species have variable numbers of ovarioles in their alate morphs?

In 1970, Michael Shaw showed that there seemed to be three types of winged black bean aphid (Aphis fabae)—migrants that flew before depositing nymphs, flyers that deposited a few nymphs before flying, and non-flyers that stayed and reproduced on their host plant. He postulated that this was an adaptation in response to host quality—the worse state the plant was in, the more likely the migrant morph would be produced. Many years later Keith Walters and Tony Dixon at the University of East Anglia, UK, showed that there was a very strong relationship between reproductive investment (number of ovarioles) and flight willingness and ability. The more ovarioles an aphid had, the less likely it was to take off and fly, and aphids with more ovarioles could not fly for as long or as far as those with fewer ovarioles. In other words, there was a trade-off between fecundity and migration. Long-distance aphid migration is very costly, with less than 0.3 per cent surviving. Therefore, it makes sense to have members of your clone taking short-distance hops (trivial flights) to neighbouring plants that might be just as bad as the one left behind and within easy reach of natural enemies, but with a higher chance of survival and reproduction, compared to long-distance migratory flights, with reduced probability of finding a host plant but which might lead to a host plant high in nutrition and low in natural enemies.

Finding the right food

An integral part of an insect’s life is finding the right place to live and feed. Living organisms need nitrogen to grow; animal tissue has the greatest concentration of this essential element, but not everyone can be a predator; someone or something has to be at the bottom of the food chain. Non-animal sources are more abundant so, despite their relative lack of nitrogen, insects mainly exploit these non-animal sources. It is a hard way to make a living, especially if your food source is plant sap, phloem (mainly sugars and some nitrogen in the form of amino acids), or xylem tissue (mainly water and minerals).

Most insects are herbivorous (or, to be pedantic, they are predators of plants) and, like other herbivorous animals, feed on the bottom trophic layer. As well as herbivores feeding on living plants, there are detritivores, feeding on the bits left behind from plants and other animals, and fungivores feeding on the fungi that abound in our ecosystems. Few are predators, although many are parasitic in some form.

Back in the 1960s, insect physiologists Mark Scriber and Frank Slansky devised a way of measuring nutritional quality of host plants for Lepidoptera, the nutritional efficiency complex, based on a number of physiological measures. Three of these measures were based on feeding and growth rate—the relative growth rate, the relative consumption rate, and the relative metabolic rate. A further three were based on measures of how the food ingested was converted from plant to insect—approximate digestibility of the food, the efficiency of conversion of the digested food, and efficiency of conversion of consumption. Through experimentation and literature review, they calculated which type of host plant was most suitable for Lepidoptera and, by inference, other chewing insect herbivores. They concluded that woody plants, trees, and shrubs were the least suitable host plants while herbaceous plants (forbs in America) were the most suitable, and that this was related to nitrogen and leaf water content (70 per cent leaf water and 8 per cent nitrogen content being optimal) and to the toughness of leaves, those of woody plants being six times tougher than those of herbaceous plants. We would therefore expect that herbaceous plants would play host to many more insect species than would woody plants, yet this is the opposite of what we see in nature. As a general rule, trees support a greater diversity of insects than do herbaceous plants. Given the poor quality of nutrition available from trees, why should this be? The answer lies in niche availability and the concept of apparency. Trees are large and easy to find, and their size and complex architecture provide a wide range of niches for insects to feed on and live in.

To feed on plants requires specialist adaptations both in terms of feeding structures and metabolic pathways. Insects that feed on leaves, fruit, and other solid structures of their host plants have chewing and biting mouthparts; those that feed from the xylem and phloem vessels have piercing and sucking mouthparts. Insects equipped with biting and chewing mouthparts also have to be prepared to deal with tissue of differing hardness/toughness. Leaves are not all equally soft (Table 4). Some plant tissues such as bark and heartwood are incredibly tough, and many insects that feed on tough tissues have incorporated metal ions into their mandibles. Plant tissue is also not equally nutritious throughout the year or the lifespan of the plant. In spring, perennial plants begin to grow and move stored nitrogen from within the plant to the growing points; annuals emerge from their seeds, soft, vulnerable, and rich in nitrogen, with a high water content. This is ideal insect fodder as many gardeners know to their sorrow. This growth phase is also extremely valuable for the plants; they need to get past this vulnerable stage as quickly as possible without losing too much of themselves to the depredations of their vertebrate and invertebrate enemies. Other insects have avoided the problems of feeding on tough leaves by emerging at the same time as their host plants burst into bud or emerge from their seeds. Many plants therefore invest in biochemical defences at this vulnerable stage of development; the young leaves of cherry trees, although tender and full of nitrogen, are also full of cyanogenic compounds. It is, however, metabolically expensive for plants to produce defensive chemicals and as the leaves grow older, tougher, and less succulent, and the plant has produced and set fruit, the need to defend the leaves chemically is reduced.

Table 4 The relative toughness of plants

Plant Type | Relative toughness
Herbaceous plants | 1.0
Woody plants—new leaves | 1.7
Temperate grasses | 3.1
Tropical grasses | 6.2
Woody plants—mature leaves | 6.3

We thus see insects that have become not only host specialists but also seasonal specialists—insects that exploit the soft, highly nutritious but well-defended young plant tissues, the flush feeders, such as the larvae of the winter moth (Operophtera brumata); those that feed on the less nutritious, tougher, but less chemically defended summer foliage; and those that exploit the more nutritious but possibly more short-lived autumn foliage, the senescence feeders. This leads on to the concept of generalists and specialists. We can classify insect species along a gradient, ranging from the extreme specialists, those that feed on only one species of host plant, to the extreme generalists, the polyphages, that feed on a disparate range of plant families. The peach-potato aphid (Myzus persicae) is often cited as being one of the most polyphagous insects on the planet, feeding on a range of plants from trees to vegetables. In between these two extremes there are the oligophagous insects, which are able to feed on a group of related plants, in either the same genus or the same family, depending on their level of oligophagy.

Although there is a school of thought that says that all insects are specialists, for the moment let us assume that specialists and generalists do exist. The first question is why? What advantages are gained from adopting each of these strategies? To be a specialist means being very well adapted to a particular host plant both in terms of season (phenology), that is, being around at the same time of year as the most nutritional part of the plant, and also being able to detoxify the host plant chemistry which the plant uses to defend itself against its predators. For example, crucifers such as cabbage are rich in sinigrin (mustard oils) that is a potent defence against many insects. Cabbage specialists, such as larvae of the diamondback moth (Plutella xylostella), or the cabbage white butterfly (Pieris rapae), have a suite of digestive enzymes that are able to detoxify these defences. Like plant defensive chemistry, a sophisticated detoxification system is metabolically expensive. If an insect has invested in one particular set of detoxification enzymes, it must sacrifice more generalist defences, so it will do superbly well when faced with a cabbage plant but will starve to death if no cabbages are available. Given that some insects are specialists on much rarer plants than cabbages, being able to find the host plant is of great importance. If, on the other hand, the insect is a generalist, it has a multi-purpose tool kit of different gut enzymes for detoxification; against some plant chemistry it works quite well, against other metabolites, less well, but in general it can cope with feeding on a range of host plants. If, however, it ends up on a cabbage plant on which a cabbage specialist is feeding, it will lose out. This is nicely shown by studies of three species of Lepidoptera: the cabbage white butterfly; the swallowtail (Papilio polyxenes), which is a specialist on parsnips; and the armyworm (Spodoptera eridania), a generalist feeding on a wide range of host plants. When fed on a crucifer-based diet, to which sinigrin was added artificially, the cabbage white grew and developed with no ill effects, even when the levels of sinigrin were three times higher than it would normally encounter, the swallowtail died, but the armyworm survived, albeit not as well as it would have done on a non-cruciferous plant. Over time, the responses of specialist herbivorous insects and the defences of their host plants evolve, an example of what is commonly termed the coevolutionary arms race.

Plants can also attempt to beat their herbivores by avoiding them in space and time. If an insect is a flush feeder, a plant that can pass through the vulnerable tender stage before the insect has emerged or arrived is at a distinct advantage. Despite their close association, it seems that insect herbivores and their host plants do not use exactly the same environmental cues to decide when to break bud or emerge from their overwintering stage.

This can have disastrous effects, as in the case of the winter moth, which has a very particular phenological niche or window, with oak foliage (Figure 10). Hatch too early and the oak is still dormant, hatch too late and the leaves are too tough for the young caterpillars to use efficiently, with many dying before completing their development, while those that survive are smaller and less fecund as adults than in years when bud burst and winter moth egg hatch coincide.

10. The ‘phenological window’ illustrated by the winter moth, Operophtera brumata. Moths that hatch too early will have insufficient food when the oak is dormant but moths that hatch too late will have to feed on tough leaves.

Whether a specialist or a generalist, as an insect larva develops it becomes more tolerant and better able to fight back against the chemical and physical defences that a plant can throw at it. Bigger jaws enable older caterpillars to chew through a thicker cuticle than newly emerged caterpillars, and their detoxification systems become more developed as they pass through successive moults. Even a specialist insect can complete its development on a ‘non-host’ plant if it is close to its final moult.

The interdependence of herbivorous insects and their host plants is echoed by their interactions with their siblings and conspecifics, an aspect explored in Chapter 4.

Chapter 4

Living together

The most basic form of insect association is exemplified by the aggregations that some insect species show during some parts of their lifecycle. Many ladybirds, for example, aggregate in sheltered spots over the winter, actively seeking out crevices in bark, the leeside of fence posts, the space underneath window sills, and the frames of sash windows. These are not truly social as they are often a mixture of different species that have come together because of a response to a change in behaviour, brought about by positive touch stimulus (thigmotaxis). Other insect aggregations that are not truly forms of sociality are seen in some Hemiptera, where feeding in groups emphasizes their unpalatability by magnifying their red and black warning colouration; colonial feeding by aphid clones where being part of a herd is beneficial; overwintering roosting behaviour of some butterflies, most famously seen in the monarch; feeding aggregations seen in some bark beetles, and similarly tent caterpillars that feed in large aggregations within protected silk webbing. In all these loose associations, any coordination is individual and, except perhaps in the case of aphids, not altruistic. They are thus solitary, but have, as a result of their behaviour, formed what to us appears to be a social aggregation.

Whereas most insects only come together to mate, feed, or overwinter, some insects have adopted a more social life. Ants, bees, wasps, and termites are well known to be social insects. Most people will be aware of the complex social organization that occurs in the hives of the domesticated honey bee (Apis mellifera). What may be less evident is that, unlike the morphological variation seen in other highly social insect groups such as ants and termites which have distinct castes, individual bees within a colony may appear very similar (that is, they show little of the phenotypic variation evident amongst ants and termites) but have marked variation in their behaviour (polyethism). Female honey bees can be divided into five castes—the queen (reproductive caste) and four age-based subcastes among the workers: cell cleaning caste, broodnest caste, food storage caste, forager caste. Newly emerged worker bees begin life as cleaners and carers; as they grow older they move further away from the centre of the hive, eventually becoming foragers. None of the workers moves abruptly from one subcaste to another but some move earlier than others because developmental rates vary among individuals. Some roles, such as undertakers and guards, are performed by a very small proportion of the colony, perhaps due to some subtle genetic differences.

In a number of species of ants and termites, there are behavioural and very obvious morphological differences among the castes, although many ant species also show similar behavioural caste differentiation to that of honey bees. Termites and ants have three main castes—reproductive (queens and kings), worker, and soldier. The former and the latter castes have smaller and larger versions, known as secondary and primary, and minors and majors, the major soldiers having very well-developed jaws. Although termites are highly social, many producing the instantly recognizable termite hills/mounds (Figure 11), and are commonly known as white ants, sharing the same caste nomenclature as ants (Figure 12), they are not Hymenoptera, but rather—and this may come as a surprise to many—they are very closely related to cockroaches. Something of a vindication for the biologist Lemuel Roscoe Cleveland, who had suggested this in the 1930s but was largely ignored.

11. A termite mound. These remarkable structures enable their inhabitants to live in a stable and relatively cool environment.

12. Termite and ant castes—note the subdivisions within castes: Ants are usually divided into three castes: reproductive females, reproductive males and non-reproductive females. Soldiers are also common within termite and ant caste systems. There is extreme variation in size and morphology amongst castes.

Social organisms need to be able to communicate with each other in order to maintain colony coherence. A major difference among ants, bees, and termites is that termites are mostly blind so whereas ants and bees are able to communicate visually, the ‘waggle-dance’ of bees being a well-documented example, communication between individual termites is mainly by touch and chemical means. In termites, as in bees and ants, this chemical communication involves pheromones that elicit behavioural responses from the individuals, including trail chemicals that lead individual foragers from food to nest and other chemicals that allow them to recognize nest mates and, of course, locate reproductive partners. These behavioural and morphological features have enabled ants, bees, and termites to reach the apex of invertebrate sociality.

Parental care

A number of other species live together in varying degrees of togetherness, some of which may come as a surprise. Leaving aside for the moment the vaguely social aggregations of aphids, the marvellous concept of ‘spaced-out gregariousness’ found in some aphid species, and the gregarious feeding habits of many lepidopteran and coleopteran larvae, parental care is found in several species not normally considered to be social.

Parental care is more common in species in which offspring face high risks due to natural enemies or environmental pressure and the mothers are longer lived than, for example, insects in which the eggs are laid in one massive clutch and the mother then dies. In the case of the flightless female of the vapourer moth (Orgyia antiqua), parental care, such as it is, involves the egg clutch being covered by her dead, unpalatable body.

Maternal provisioning, in which the mother leaves a prey item with each egg, is common in solitary bees and wasps. The ability of some moth and butterfly species to lay eggs with more nutritional reserves on poorer quality host plants is perhaps not what would normally be termed maternal care. More recognizable maternal care is seen, for example, in some dung beetles, where the parents feed their offspring in response to ‘begging’ behaviour, similar to that seen in birds. Many dung beetles share parental responsibility; females excavate brood chambers and lay eggs in the dung-ball food source while the males bring dung for the females to deploy as necessary. This type of behaviour is known as subsociality.

The silphids (carrion and sexton beetles), which feed on dead animals, also show parental care and male/female cooperation. In some circumstances they also show quasi-social behaviour. In a series of elegant trials, Stephen Trumbo and David Wilson demonstrated that in some contexts, such as when the carcass is large, the females, which are normally highly competitive, form cooperative breeding associations, leading to better survival rates of their offspring.

The earwig also provides a good example of subsocial behaviour, tending her eggs carefully, protecting them from predators, and staying with the newly hatched larvae until their second moult, when they can fend for themselves. If the mother earwig dies before her parenting role is complete, the nymphs will eat her dead body before they disperse.

True bugs, perhaps not commonly regarded as being advanced enough to exhibit parental care, do however, provide many examples of this behaviour. Female burrower bugs (Sehirus cinctus) show extended care for their offspring; they guard their clutch and feed the hatched nymphs up to the third larval instar. Hungry nymphs use a pheromone to solicit food from their mothers. Another hemipteran, the membracid oak tree hopper (Platycotis vittata), guards her eggs and, in response to vibrational signals from her offspring, chases predators, including ants, away. Similar to vertebrate mothers, they also keep their nymphs in aggregations, herding straying offspring back into the group. And the hemipteran Parastrachia japonensis, a species of true bug from eastern Asia, keeps watch on her eggs and moves them to new sites if they become flooded or are in danger of desiccation.

Aphids and their soldiers

Perhaps more remarkable and hardly known outside the world of aphidologists are the subsocial aphids. The phenomenon is not common, being found only in about 1 per cent of aphids. It was only discovered in the 1970s, and was viewed initially with some scepticism. Among aphids, the Pemphigine aphids are renowned for their gall-forming activities, many galls being formed along the leaf petiole. The position of the gall is very important; the closer the gall is to the base of a leaf, the better the quality of the food for the gall inhabitants. There is thus a premium to be gained by either being first to form a gall or, if in second place, to usurp the aphid mother that got there first and push her further up the leaf petiole. We thus see two strategies. Newly emerged first-instar nymphs of the beet aphid (Pemphigus betae) fight each other for the best position on the petiole (Figure 13). These fights are serious affairs and, incredibly, can last for up to two days. And in a related species, Epipemphigus niisimae, where a gall has already been formed by an earlier arrival, the first-instar nymphs fight to gain possession of this premium dwelling place. These fights are even more vicious and protracted and the Japanese entomologist Shigeyuki and colleagues reported that they sometimes result in the death of the loser.

13. Japanese fighting aphids ‘Ninja aphids’. In (a) they are fighting rear to rear, in (b) head on.

As a further development, some gall-forming aphids, Ceratoglypnia styracicola and Hamamelistes cristafolaie, have a specially adapted nymphal morph, with thicker and broader front legs, whose function is to defend gall usurpation by other aphid mothers, so-called soldier aphids. These soldiers stay outside the gall and repel possible invaders. So, it is not surprising to find that in some species, the soldiers do not just fight other aphids but actually defend their siblings against predators, even being able to kill lacewing larvae.

Ant–insect–plant associations

The relationship between ants and sap-feeding insects, such as aphids, has long been recognized. The first scientific description of this phenomenon was by the 17th-century Dutch naturalist and painter Jan Goedaert, and by the latter half of the 19th century the phenomenon was well known, appearing in many popular science books of the time, including Ernest van Bruyssel’s excellent and very readable book, The Population of an Old Pear Tree (1870).

The ant–aphid association is usually defined as a mutualism, as the two species exist in a relationship in which each benefits from the activity of the other; it is also sometimes termed trophobiosis, which is a more symbiotic relationship.

We tend to think of aphids as soft, defenceless insects that are easy to squash when we find them on our house and garden plants. To predatory insects, however, they present a bit more of a challenge. Aphids have structural and behavioural defences to keep them safe in the dangerous world of bug eat bug. Alarm pheromones and the seemingly dangerous habit of simply dropping off a plant (dropping behaviour) when a predator approaches are commonly used by aphids to avoid meeting predators face to face. Aphids also have a number of physical defences: their siphunculi, or cornicles, tubules that protrude from the back of their abdomen, can produce a quickly hardening wax to gum up ladybirds’ jaws. Other aphid species cover themselves with dense waxy coats that make them less palatable or accessible to natural enemies. Yet others have thick skins (heavily sclerotized) and what entomologists term saltatorial leg modification (long legs), and are able to give a ladybird or other insect predator a good kicking. These characteristics, which are all costly, are reduced or absent in aphids that are associated frequently with ants; presumably with ant bodyguards in attendance, there is no need for the aphids to invest in extra anti-predator defences.

The degree of dependence of the aphid on the ants varies by species. Some aphids, especially those that live underground on plant roots, are unable to survive without their ant attendants. The entomologist John Pontin describes seeing yellow meadow ant (Lasius flavus) workers licking aphid eggs, which he suggested stops them from going mouldy by removing fungal spores. He noted that eggs that were not cared for in this way did not hatch. Other aphids have a more facultative relationship, and are able to survive quite successfully without the help of their friendly neighbourhood ants.

Apart from reducing their defensive armoury, aphids that have obligatory ants in attendance have a specially adapted rear end, essentially a hairy bottom, known more scientifically as the trophobiotic organ (Figure 14). This organ is an enlarged anal plate surrounded by special hairs that acts as a collection and storage device, allowing the aphid to accumulate honeydew (aphid equivalent of faeces): a mixture largely composed of sugars, but also of free amino acids and amides, proteins, minerals, and B-vitamins, which is, all in all, quite a useful food source for the ants, ready for the ants to remove at their leisure. Trophobiosis is a symbiotic association between organisms in which food is obtained or provided. The provider of food in the association is referred to as a trophobiont. The name is derived from the Greek τροφή, trophē (nourishment) and βίωσις, biosis (short for symbiosis).

14. Three aphid trophobiotic organs, some hairier than others.

Non-ant-attended aphids without the trophobiotic organ deposit their honeydew directly onto the leaf surface, the ground, or, if you are unlucky enough to park under an aphid-infested tree, your car. Ants lick and collect sycamore aphid (Drepanosiphum platanoidis) honeydew from leaves but not directly from the aphids, although they will collect honeydew directly from the maple aphid (Periphyllus testudinaceus), which also lives on sycamore trees.

So what’s in it for the ants? Why do they bother looking after aphids, even in some cases keeping aphid eggs in their nests through the winter? The obvious answer is: for the honeydew that the aphids produce. The amount of material that an aphid can remove from a plant is quite astounding: a large willow aphid (Tuberolachnus salignus) adult can imbibe the equivalent of 4 milligrams (mg) sucrose per day, equivalent to the photosynthetic product of one to two leaves per day. Admittedly, they are large aphids and not ant attended, but even an aphid half their size passes a lot of plant sap through its digestive systems. All aphids produce honeydew but not all aphids are ant attended and, as pointed out earlier, not all ants attend aphids. My research group found that 41 per cent of ant genera have trophobiotic species, but these are not distributed equally among ant families. Some ant subfamilies, such as the Formicinae, specialize in ant attendance, whereas in other ant families aphids are used only as prey and the honeydew is gathered from plant and ground surfaces. The ant species that are most likely to develop mutualistic relationships with aphids seem to be those that live in trees, have large colonies, are able to exploit disturbed habitats, and are dominant or invasive.

Ants that do tend aphids do not just protect them from predators and other natural enemies; they also seek to maximize the return for their investment. The black bean aphid, which is often tended by the black garden ant (Lasius niger) has its ability to produce winged forms reduced by the ants, thus making sure that the aphids are around for longer to provide food for them. The ant Lasius fuliginosus transports young giant oak aphids (Stomaphis quercus) to parts of the tree with the best honeydew production; Lasius niger goes one step further, moving individuals of the black willow bark aphid (Pterocomma salicis) to better quality willow trees. Lasius niger seems to have a propensity for moving bugs about; it has also been seen moving scale insects from dying clover roots to nearby living roots.

In the mid-1970s John Whittaker and Gary Skinner of Lancaster University, UK, studied the interactions between the wood ant (Formica rufa) and the various insect herbivores feeding on sycamore trees in Cringlebarrow Wood, Lancashire. They excluded some ants from some of the aphid-infested branches and allowed them access to other branches on the same trees; they also looked at trees that were foraged by ants and those that were not. They found that F. rufa was a heavy predator of the sycamore aphid, but tended the maple aphid. Ant-excluded colonies of the maple aphid decreased while those of the sycamore aphid did not; the reverse pattern was seen on branches where ants were able to access the aphids.

The presence of thriving aphid colonies in the neighbourhood of ant nests (and in some cases aphid colonies only exist near ant nests) has made some people wonder whether aphids look actively for ant partners. There is no evidence for this but the fact that wing production is reduced in the presence of tending ants means that aphid colonies can accumulate around and close to ant nests.

That does not mean that the aphids rely only on honeydew production to guarantee the presence of their ant bodyguards. The aphid Stomaphis yanonis, which, like other Stomaphis species, has giant mouthparts, needs plenty of time to remove its mouthparts safely and definitely needs ant protection when involved in the delicate operation of stylet unplugging. In this case, it turns out that the aphids smell like the ants. The skin of these aphids has cuticular hydrocarbons that resemble those of their ant protector Lasius fuji, which encourages the ants to treat them as their own. Earlier work on the ant-attended tree-dwelling aphids, Lachnus tropicalis and Myzocallis kuricola, in Japan showed that the ant L. niger preyed on aphids that had not been attended by nest mates but tended those that had previously been tended. This too would indicate the presence of some sort of chemical marker or brand.

Although aphids do not seek ant partners actively, they may compete with each other to retain the services of their ant bodyguards by producing more honeydew. Christophe Fischer and colleagues from the University of Liège, Belgium, showed that ants decide whether to predate or tend aphids by monitoring honeydew production and choose to prey on aphids in colonies that produce less honeydew. They have also shown that the honeydew of the black bean aphid (Aphis fabae) is often colonized by the bacterium Staphylococcus xylosus. Honeydew so infected produces a bouquet of volatile compounds that are attractive to the ant L. niger, thus increasing the chances of the aphids being ant attended. This adds yet another layer of complexity to the already complicated mutualistic lifestyle that aphids have adopted.

Finally, although the wonderful colour variations seen in some aphid species can be modified by their symbionts, it seems that ants may have a say in this too, albeit at a colony level rather than at the clonal level. The improbably named mugwort aphid (Macrosiphoniella yomogicola), which is obligately ant-attended by Lasius japonicus, is found in colonies that are typically composed of 65 per cent green aphids and 35 per cent red aphids. Saori Watanabe and his colleagues at the University of Hokkaido, Japan, questioned why ants like this colour balance. One possibility is that red and green aphids have slightly different effects on the mugwort plants where they feed. Though green aphids produce more honeydew, red aphids seem to prevent the mugwort from flowering. Given that aphid colonies on a flowering mugwort go extinct, ants looking to maintain an aphid herd for more than a year might see an advantage in keeping red aphids around to guarantee a long-term food supply from their green sisters.

Ants and plants

As well as ‘farming’ aphids to obtain sugar from their honeydew, ants have a similar mutualistic relationship with plants that give them a sugary reward to protect them from herbivorous insects, except those that also provide the ants with sugar. Perhaps the most studied, familiar ant–plant mutualism is that of the swollen-thorn acacia and Pseudomyrmex ants, which American ecologist Dan Janzen described in the mid-1960s. In essence the swollen thorns of the acacias provide housing for the ants and an additional reward via extra-floral nectaries. In return the ants drive away insects and other herbivores. Such mutualisms are not just confined to the tropics or single plants; they can be very sophisticated, as ecologist Dave Tilman showed in the 1970s. In Michigan, the North American black cherry, Prunus serotina, times nectar production from its extra-floral nectaries to attract the ant Formica obscuripes when the larvae of its major herbivore, the eastern tent caterpillar (Malacosoma americanum) are at their most vulnerable. Protected trees have greatly reduced levels of herbivory. When more than one ant colony is involved, rather than single trees being protected, a group of trees can be saved from defoliation, and form a green island. The areas covered by green islands can be quite extensive: two ant colonies of the ant Formica polyctena were enough to protect pine trees from the nun moth (Lymantria monacha) in Sweden within a 45 m diameter around the colonies (0.16 hectares (ha)) and green islands of up to 3 ha have been reported. Finnish entomologists reported that one colony of the ant Formica aquilonia was sufficient to create green islands of subarctic mountain birch, Betula pubescens, of up to 0.12 ha.

Insects and their symbionts

Many insects, especially those feeding on nutrient-limited diets, like blood, wood, phloem, and xylem, need help in obtaining essential nutrients. Termites, for example, have a mutualistic relationship with protozoa and bacteria that enables them to process cellulose, and bed bugs need the help of Wolbachia bacteria to process their blood meals. Recent evidence has revealed that both termites and bedbugs have symbionts that confer defence against disease; this is especially relevant in female bedbugs as many potentially harmful bacteria are introduced via the male method of traumatic insemination. To my mind, however, the most interesting and, to date, most extensively studied symbiotic/mutualistic relationships are found in aphids.

Like humans, aphids have a thriving internal ecology; they are inhabited by a number of bacteria or bacteria-like organisms. The existence of these fellow travellers and the fact that they are transmitted by the mother has been known for over a century: Thomas Henry Huxley first described them in 1858, although he had no idea what they were. The Czech entomologist Jaroslav Peklo (1881–1955) proved in 1912 that they were bacteria but their role within the body of the aphids was not entirely understood until, some years later, the Hungarian entomologist László Tóth hypothesized that because the plant sap that the aphids feed on did not contain enough proteins to meet their demands for growth, they must be obtaining the extra nitrogen that they needed from their symbionts.

To demonstrate this, entomologists treated insects with antibiotics and proved that the symbionts were, first, bacteria; and, second, that they provided benefits for their insect hosts. They concluded that there was enough evidence to suggest that the endosymbionts were involved in some way in the nutritional and possibly reproductive processes of the insects studied—mainly cockroaches. A few years later two American entomologists sprayed aphids with several different antibiotics and found that this caused increased mortality and reduced fecundity compared with untreated aphids. Further studies on other aphid species showed that the antibiotics eliminated and damaged their symbionts and that once ‘cured’, aphids developed more slowly, if at all, and produced fewer offspring. Yet more evidence that the symbionts were an essential part of the aphid biome. There was still much debate as to how the symbionts provided proteins to the aphids, a question that remained unanswered until the 1980s. Rosalind Hinde and colleagues were able to show that material produced from the symbionts was passed into the body of the aphid and that the primary symbionts were able to synthesize amino acids and sterols for the benefit of their aphid hosts (partners). By the early 1980s it was accepted that aphids were unable to reproduce or survive without their primary symbionts; and, by the late 1980s, that dietary sterols were provided by the primary symbionts.

Despite the huge amount of research and the general acceptance that the endosymbionts were an integral part of the aphid’s biome, their putative identity was not determined until 1991, when they were named Buchnera aphidicola and given their own genus; note, however, that B. aphidicola represents a complex of closely related bacteria rather than a single species. It was soon confirmed that they were responsible for the synthesis of essential amino acids used by the aphids, such as tryptophan, and that it was definitely an obligate relationship on both sides.

Next, attention turned to the presumably facultative secondary symbionts, first noticed in the rose aphid (Macrosiphum rosae) more than twenty years earlier by Rosalind Hinde. Nancy Moran and colleagues at the University of Arizona, USA, identified three species of secondary bacterial symbiont, Serratia symbiotica, Hamiltonella defensa, and Regiella insecticola. As these are not found in all individuals of a species, they are facultative rather than obligate. The secondary symbionts were shown to be linked to a whole swathe of aphid life-history attributes, ranging from resistance to parasitoids, resistance to heat and other abiotic stressors, and to host-plant use.

Like a number of other aphid species, the pea aphid (Acyrthosiphon pisum) occurs in different colour morphs ranging from a pale green to deep reddish-pink. Tsutomo Tsuchida and colleagues in Japan showed that the intensity of green colouration depends on the presence of yet another endosymbiont, a Rickettsiella. They hypothesized that being green rather than pink or red may reduce predation by ladybirds, as the aphids would be less obvious on the leaves.

New secondary symbionts continue to be discovered and new hypotheses are raised and tested. There seems to be a whole ecology of secondary symbionts within the aphid biome waiting to be explored and documented.

Green islands

Some insects, such as aphids, induce early leaf senescence to improve the quality of their host plant (the nitrogen content of senescent leaves is higher than that of mature leaves). Some plants induce senescence and early leaf-fall in leaves that have been colonized by gall aphids in order to reduce their infestation load. Other insects try desperately to prevent senescence in order to prolong their feeding life on what would otherwise be a dead leaf (Figure 15).

15. Green island leaf-mine of the moth Stigmella atricapitella.

The phenomenon of the green islands in autumn leaves associated with leaf-mining Lepidoptera has been known for some time, but, although the adaptive value of this was easy to understand, the causal mechanism remained unknown for some time.

Plant pathologists had known since the 1930s that fungi produced secretions containing plant growth substances, such as the auxin (plant hormone) indole acetic acid. They hypothesized that the levels present in the surrounding leaf tissue were associated with the resistance or lack thereof to the fungal agent. A further class of plant growth substances, initially termed kinins because of their similarity to kinetin (a cell growth promoting plant hormone) but later renamed cytokinins, were discovered in the 1960s by Folke Skoog and co-workers and linked to the production of green islands by plant pathogens.

How does this relate to leaf-mining insects? Lisabeth Engelbrecht, working on nepticulid leaf-miners on birch, Betula pendula, and aspen, Populus tremula, set up a study in the mid-1960s to test the hypotheses that the green islands were caused by insect saliva or by the larvae physically cutting the leaf veins that would otherwise have delivered the chemical signal responsible for beginning leaf senescence. She discovered that the green islands contained large concentrations of cytokinin and, with other colleagues, discovered that the labial glands of leaf-mining larvae also contained cytokinin. In the mid-2000s the French entomologist David Giron and colleagues showed that the leaf-miner Phyllonorycter blancardella manipulates the nutritional quality of its host leaves by increasing the levels of cytokinin in the surrounding leaf tissue.

As we know from aphids, where insects play, bacterial symbionts are never far away, and sure enough it wasn’t long before it was shown that Wolbachia ‘infections’ were helping leaf-miners to produce their ‘green islands’. Wilfried Kaiser and colleagues treated leaf-miner larvae with antibiotics to remove the symbiont and found that the ‘cured’ larvae, although still able to feed and form leaf-mines, were unable to produce ‘green islands’, and the levels of cytokinin were much lower than those found in the ‘green islands’ formed by untreated leaf-miners (Figure 16).

16. Influence of Wolbachia on green island formation: (left) infected leaf-miners, Phyllonorycter blancardella, surrounded by nutritious plant tissue; (right) ‘cured’ by antibiotics, the leaf-miner soon runs out of food.

In Chapter 5 we leave the terrestrial habitat to explore the adaptations and lifestyles of insects that spend some or all of their life in or on water.

Chapter 5

Aquatic insects

Aquatic insects, adaptations, the marine environment

Although largely terrestrial, insects have not abandoned the world of water. Every inland water body, whether a river, stream seepage, or lake, supports a biological community. Insects can also be found in puddles and some, such as the pitcher plant mosquito, Wyeomyia smithii, are especially adapted to exploit the water-filled ‘stomachs’ of carnivorous plants. In larger water bodies, the most familiar inhabitants are often the vertebrates, such as fish and amphibians. At the macroscopic level, however, invertebrates provide the highest number of individuals and species, and the highest levels of biomass and production. In general, the insects dominate freshwater aquatic systems, where only nematodes can approach them in terms of species numbers, biomass, and productivity. Crustaceans may be abundant in saline (especially temporary) inland waters but are rarely diverse in species. Some representatives of nearly all the orders of insects live in water and there have been many invasions of freshwater from the land. Recent studies have even revealed a diversity of aquatic diving beetles (Dytiscidae) in aquifers (underground water bodies). Insects, however, have been almost completely unsuccessful in marine environments, with a few sporadic exceptions such as some water-striders (Hemiptera: Gerridae) and larval dipterans.

There is little doubt that insects evolved on land, albeit from an aquatic crustacean ancestor (Chapter 1). The tracheal system of respiration, based on diffusion, is very unlikely to have evolved in water; oxygen levels are much lower in water than in air, reaching only 15 parts per million (ppm) even in flowing water. It is much more plausible that the tracheal system facilitated the subsequent development of the ‘gills’ used by insects that are truly aquatic for part or all of their lifecycles.

Many insects have aquatic larvae, such as dragonflies, mayflies, and several species of fly, including mosquitoes. There are also some adult forms, mainly predators, that make a living in these environments, either below the surface or striding or skating across the surface. Insects that live on the surface of the water—water boatmen and pond skaters—rely on the fact that their light weight and limited contact with the water surface keeps them high and dry. Insects that feed in water but are otherwise terrestrial have special adaptations that allow them to spend prolonged periods of time underwater. Adult diving beetles store air underneath their wing cases while other semi-aquatic insects encase themselves in a bubble of air, which they refresh as needed by returning to the surface.

Insects that are truly aquatic have developed gill-like structures—fine filamentous, thin-skinned outgrowths that are able to absorb oxygen through diffusion. They depend, however, on being in a well-aerated water body or having the ability to generate a flow of fresh water over their gills, as seen in some of the ‘sedentary’ caddisflies that live in a ‘burrow’ and use their legs to produce an artificial current.

Other aquatic insects with an open spiracle system, fly larvae such as mosquitoes, and rat-tailed syrphid maggots maintain contact with the water surface with a siphon and use atmospheric oxygen. Some mosquito larvae (Mansonia spp.) can pierce the roots of aquatic plants and use the oxygen in the air pockets.

Insects with closed spiracle systems are unable to rely on simple cutaneous diffusion except at very early larval stages, and in these we see the development of structures based on external extrusions of the tracheal system. These are analogous to gills as they have a large surface area, are moist and vascular, and can be ventilated. In dragonflies and mayflies, they have been shown to account for up to 70 per cent of oxygen uptake.

Modes of life in water

Aquatic insects can be divided into six functional groups: shredders, collectors, scrapers, piercers, predators, and parasites.

Shredders feed on living or decomposing plant tissues, including wood, which they chew, mine, or gouge. Shredders break down large particles of plant material into smaller pieces that are transported downstream or made available to other stream consumers. This group includes stoneflies (Plecoptera), caddisflies (Trichoptera), and crane flies (Diptera).

Collectors feed on fine particulate organic matter by filtering particles from suspension or fine detritus from sediment; gatherers collect from the stream bottom; and filterers collect fine particulate matter from the water column. This group includes several subfamilies of chironomid midge. Filterers have special adaptations to capture particles directly from the water column. These include the construction of nets to filter water like those used by some Trichoptera larvae. Even though some Trichoptera catch animals in their nets and would therefore be classed as predators, functionally they are still considered collector-filterers. As well as the Trichoptera, this group (Collectors) includes mayflies, stoneflies, midges, and blackflies.

Scrapers feed on attached algae and diatoms by grazing solid surfaces. This group includes mayflies and caddisflies.

Piercers feed on cell and tissue fluids from vascular plants or larger algae, by piercing and sucking the contents. An example is Hydroptilidae, a tiny caddisfly species that pierces individual algal cells to consume cellular fluids, avoiding consumption of cellulose-rich cell walls.

Predators feed on living animal tissues by engulfing and eating the whole or parts of animals, or piercing prey and sucking body fluids. They use a diversity of strategies for capturing prey, including modified mouthparts and behaviour. Although many predators have abundant, strong teeth for prey consumption, some are highly specialized: the labium in Odonata, for example, is a highly modified, unique structure among aquatic insects. This group also includes one species of mayfly and one group of caddisflies.

Parasites, or more properly parasitoids (Chapter 8), complete their development within a number of aquatic larvae, for example the hymenopteran Agriotypus armatus that parasitizes caddisflies. The adult female walks down plant stems to search the stream bottom for suitable hosts. Another wasp, the egg parasitoid Pseudoligosita longifrangiata, lays its eggs within the eggs of the damselfly Argia insipida, which it finds on submerged leaves of the tropical aquatic plant Tonina fluviatilis (a common aquarium plant). And the tiny trichogrammid wasp Trichogramma julianoi parasitizes eggs of the aquatic fly Sepedon fuscipennis.

Although several orders of insect, including the Coleoptera, Diptera, Neuroptera, Megaloptera (alderflies), and the Hemiptera, have species that are aquatic, there are four orders in which almost all members spend their larval life underwater—the Ephemeroptera (mayflies), the Plecoptera (stoneflies), the Odonata (dragonflies, damselflies), and the holometabolic Trichoptera (the caddisflies). These orders are of particular importance to both the aquatic ecosystem through their various activities, and to humans as environmental indicators of water quality.

The Ephemeroptera

Worldwide there are estimated to be about 2,500 species of Ephemeroptera, commonly called mayflies, or, less commonly, dayflies. As the latter name suggests, the adults live for only a short time, a few days at most. They do not feed, having non-functional mouthparts, although some species will take on water. Their guts are filled with air and many species have vestigial legs. The sole function of the adults is to mate and for the females to lay eggs.

The immature stages (nymphs) are aquatic, and, depending on species, take one to three years, with up to fifty moults, to reach adulthood (Figure 17). The nymphs are mainly herbivorous, feeding on algae, or detritivorous, feeding on decaying material; they provide a food source for many predators. A few species are predators, with chironomid midge larvae and other small aquatic larvae as their prey. Mayflies are unique in that they have a short-lived, winged pre-adult stage, the subimago, known to anglers as the dun, which, once emerged from the water, flies to a sheltered spot where it rests for a short while before moulting yet again to become the full adult. Many species emerge synchronously, although contrary to popular belief, not all species do so in the spring, some species having autumn swarms. The mass emergences are probably an adaptation to their short lifespans, enabling mating swarms to form. The females enter the swarms, copulate in flight, and lay their eggs either directly on the water surface or on submerged vegetation. The number of eggs laid ranges among species, from a modest 400 to an astounding 3,000. Some mayfly species are also facultatively parthenogenetic, meaning that unfertilized eggs are able to produce viable larvae; this may be an adaptation to their short adult lifespan and limited dispersal ability as they are weak flyers.

17. Generalized lifecycle of a mayfly (Ephemeroptera).

The Plecoptera

The Plecoptera, or stoneflies, number approximately 4,000 species. They are found on all continents except Antarctica, mainly along stream margins or lake shores; about half the species are found in Asia and only about 150 in Europe. The common name may reflect the fact that larvae are often found under stones in streams and rivers. The adults are all terrestrial with one exception, Capnia lacustra, which has only been found at depths of 60–80 m in Lake Tahoe. Like the mayflies, the larvae of stoneflies, which are all aquatic, are extremely intolerant of pollution, have a very high oxygen requirement, and are most often associated with running or well-aerated water. The larvae resemble the adult forms very closely but have gills and no wings (Figure 18).

18. Larval and adult forms of the Plecoptera. Note the gills in the larval stage and absence of wings.

Stoneflies are temperature limited, with an upper thermal threshold of 25oC. Their very narrow habitat requirements and poor dispersal ability mean that they are probably one of the most endangered groups of insects globally, surpassed only by the ice crawlers (Chapter 7).

The larvae have generalized biting mouthparts, and feed on dead and decaying plant material and other organic detritus. Some species are carnivorous and tend to specialize on particular prey items as they age.

The adults emerge at night, mainly in the spring or early summer, but some species emerge in the autumn. They are protandrous—the males emerge and mature before the females and die soon after copulation. Surprisingly little is known about the ecology and biology of the adults. They have functional mouthparts, and the females live for longer than the males. As they need to mature before laying eggs, they, unlike the very short-lived males, almost certainly need to feed; it is thought that they may feed on lichens. Depending on species, the eggs are either dropped onto the surface of the water or laid on submerged vegetation. In both cases, the eggs have a sticky surface that is activated on contact with water. Some species lay up to 1,000 eggs; they vary greatly in size, from 5 to 50 µm, and, ranging in colour from black to green or yellow, they are often marked with distinctive light or dark patterns. Some species are wingless, but most are winged although they are poor flyers. Their hind wings have an expanded posterior lobe that folds longitudinally under the main wing, giving them their characteristic appearance when at rest (Figure 18).

The Odonata

Everyone is probably familiar with the Odonata, the dragonflies and damselflies. There are about 6,300 species, again found on all continents except Antarctica. They are ancient insects: fossil records of their ancestral group, the Protodonata, date back to at least as far as the Upper Carboniferous (Pennsylvanian) sediments in Europe, formed about 325 MYA. The Protodonata were fast-flying insects with spiny legs and wingspans up to 75 cm. This group went extinct in the Triassic, about the time that dinosaurs began to appear.

Odonates use their wings in a unique manner. Other four-winged insects beat them synchronously, but dragonflies can beat the fore and hind pairs independently, allowing three different modes of flight in which the pairs beat synchronously, alternately between the two sets, or synchronously but out of phase with each other. This allows odonates to display a variety of aerial aerobatics, including hovering, backward flight, and the ability to turn on a mid-air pivot. No wonder they are such good predators.

Adult and larval odonates are generalist predators: they eat whatever suitable prey is abundant and catchable. Their main diet is small insects, especially flies, but they will also take advantage of termite, ant, and mayfly swarms, sometimes hunting in groups. Adult dragonflies do not hunt in cold weather, unlike damselflies, which have a lower temperature threshold. As with many other insect species, the odonate males are territorial and patrol their areas, which can extend some distance from water sources as they are very strong flyers, unlike other aquatic insects. Except for a few Hawaiian damselflies which have terrestrial larvae, most return to their aquatic habitats, where they lay their eggs in or very near water. The eggs hatch shortly afterwards and the larvae emerge in the water or crawl into it as quickly as they can.

Once hatched they begin to feed and grow. Another difference between dragonflies and damselflies is the length of their larval (nymphal) period. Whereas most damselflies complete their larval development within a year, most of a dragonfly’s life is spent in the larval stage, moulting from six to fifteen times; some complete this within one or two years while others can take as long as six years, varying according to altitude and latitude. The aquatic larvae are very different from the terrestrial adults (Figure 19). Wing buds begin to show about halfway through the developmental period.

19. Larval stages of a dragonfly.

Like the adults, the larvae (nymphs) are voracious predators. The early instars feed on small prey items, such as crustaceans and protozoans. The later instars graduate to larger animals including snails, water beetles, and even small fish. Although they are ferocious predators, they too can fall victim to predators and provide a valuable food source for a range of amphibians, reptiles, and birds; they also host a range of parasites. If they survive to their final instar, the nymphs crawl out of the water and moult into the winged adult with which we are all familiar.

Despite their beauty, in folklore dragonflies are often associated with the devil. As well as helping the devil weigh and measure souls, they were also reputed to sew up the mouths of naughty children—hence the devil’s darning needles—and to make people blind and deaf, with their claspers being the needles and pokers. One of the common names in Romania is St George’s Horse, which, according to legend, was the devil transformed into a giant dragonfly.

The Trichoptera

Except for specialists, most people tend not to give much thought to caddisflies; if they know anything about them, it is probably limited to the fact that they are aquatic and live inside a case of bits of vegetation, particles of sand, or small pebbles, spun together with silk thread. As a child I discovered that if I very carefully removed the case from a larval caddisfly and reared it in an aquarium with a suitable food supply and a range of different substrates, such as coloured sand and pebbles, I could end up with a technicoloured caddis case. This attribute has been used by canny entrepreneurs who sell very expensive caddis jewellery.

The origin of the word ‘caddis’ is unclear, but it dates to at least Izaak Walton’s The Compleat Angler (1653), in which ‘cod-worms or caddis’ are mentioned as being used as bait. Thomas Muffet (Moufet) used the term cados worm in his book Insectorum sive Minimorum Animalium Theatrum (‘great variety of cados worms’), which was published posthumously in 1658 (Muffet died in 1604). The term cadyss was used in the 15th century for silk or cotton cloth, and ‘cadice-men’ were itinerant vendors of such materials but a direct connection between these words and the insects has not been established.

Most people probably would not recognize an adult caddisfly; and those who do usually think that they are some sort of moth. This is actually quite a sensible guess as evolutionarily speaking the Lepidoptera and Trichoptera are closely related and are in the same super-order, the Amphiesmenoptera. Trichoptera literally translates as hairy wings, Lepidoptera as scaly wings, and many adult caddisflies look remarkably similar to micro-moths.

The majority of caddisflies have aquatic larvae although there are a few that have become completely terrestrial and spend their lives foraging in damp leaf litter and hiding in bark crevices. The adults lay their eggs in water, on aquatic vegetation, or on nearby trees. On hatching, the larvae go through several (usually five) moults before pupating. The adults emerge in spring or early summer.

Caddisflies are probably the most successful of the aquatic insects. Data from stream surveys frequently list as many species of Trichoptera as species of Ephemeroptera, Odonata, and Plecoptera combined. Their success can be put down to their use of silk and ability to exploit a range of aquatic habitats. They can live in running water, or in ponds and lakes. Some of the ‘ponds’ can be very temporary, such as puddles, or pools formed in plants such as bromeliads. As we noted earlier, insects that live in running water are well supplied with fresh, aerated water while those living in ponds and pools have to make their own currents by flexing their bodies and moving their legs, in order to pass ‘fresh’ water over their gills. Sedentary caddisfly larvae live in fixed shelters and use silk ‘fishing nets’ to catch their food (Figure 20). Those that live in fast-flowing streams have coarse, tight nets. Insects living in slow-flowing streams use baggy, fine-grained nets.

20. Caddisfly fishing net.

Some caddisfly larvae are free-living foragers with portable cases. Like other insects, they use silk, leaving a thread behind them, to attach themselves to the substrate so that they are not floated downstream willy-nilly. If they live in fast-flowing streams their cases are streamlined.

As well as the very few terrestrial caddisflies, another family of caddisflies, the Chathamiidae, deserve a mention, being one of the few insects that have returned to the marine environment, although only to the tide line. These marine caddisflies are case bearers and found only in Australasia. The larvae feed on algae and live in deep rock pools with a connection to the open sea and, unlike their terrestrial and freshwater relatives, the adults do not have a synchronous emergence phase, emerging instead over a period of several months.

Marine insects

Having emerged, via a cave-dwelling crustacean ancestor, from the sea about 400 MYA, insects seem to have been reluctant to return there. Of the 1.2 million insects so far described, a mere 30,000 to 40,000 species, 3 per cent or so, are aquatic or have aquatic larval stages. Of these, about 9,000 species (mostly bugs and beetles) spend their entire lifecycle under or on water. In about 30,000 species, the flies, mosquitoes, mayflies, caddisflies, dragonflies, only the larval stage is aquatic. Although the oceans cover something like 75 per cent of the Earth’s surface, insects are relatively absent from this habitat. Why, apart from a few exceptions, which I will mention later, are insects so scarce in the marine environment?

Dr Lanna Cheng, of the University of California, San Diego, suggested the following ideas. First, the marine environment is salty, and it is possible that insects are limited by this salinity. This may be true for most insects but, thanks to their highly efficient osmoregulatory system, some fly larvae are able to tolerate salinity in excess of three times that of the ocean. Second, the ocean is deep, which stops insects from completing their development. Again, this is true for many insects but there are flies, such as chironomid midge larvae, that are found at depths (2,500 m) below those that even the deepest-diving whales can reach. Third, the combination of ocean depth and salinity makes the oxygen content of such habitats too limited for insect survival, but, once again, some fly larvae can survive months without oxygen. Indeed many other aquatic insects survive, if not thrive, in polluted waters with similar or lower oxygen concentrations to those found in the ocean depths. The final, and perhaps most compelling, hypothesis concerns crustacean competition. If we argue that insects are so successful because they colonized land, then by moving away from the ocean, they exploited and adapted to a terrestrial existence, while their major competitors, the crustaceans, stayed in the sea and continued to adapt to that environment. Now, millions of years later, insects are unable to compete successfully in the ocean and their distant crustacean cousins have similar difficulties on land. Professor Cheng is a strong advocate of this hypothesis and points out that the only insects that live in the open ocean live on its surface and never meet the crustaceans living beneath its surface. Other explanations for the paucity of truly marine insects are that the difficulty of living at depth because of their air-filled tracheal system makes them much more vulnerable to predation by fish; and, additionally, it is difficult to produce aerial dispersal stages in an ocean environment. Freshwater insects are able to use semi-submerged vegetation as platforms for their newly moulted adult stages to first break the surface tension to emerge above the water and secondly to rest upon while their wings unfold and harden prior to flight. In the open ocean such structures are extremely rare. This combination of factors goes some way to explaining the lack of underwater dwelling marine insects.

There are in fact several hundred insect genera in fourteen orders associated with marine shoreline environments but only members of the genus Halobates, the sea or ocean skaters, are found in the open seas. These are Hemiptera in the family Gerridae and were discovered almost 200 years ago by Johann Friedrich Gustav von Eschscholtz during his voyage on the Russian expeditionary ship Rurik between 1815 and 1818. Although 90 per cent of gerrids are freshwater dwellers, there are forty species within the genus Halobates, five of which are truly marine. They are distributed in all tropical oceans between 40 N and 40 S. Gerrids are fascinating in their own right: witness their ability to skim across the surface of ponds and streams. Gerrids also have some interesting facets to their biology and ecology. They have short- and long-winged forms, use ‘ripple communication’, basically causing waves to attract mates, and some species show territorial behaviour and mate guarding. Halobates is, however, the only genus with species that are wholly oceanic. These are remarkable insects indeed; they have a tropical distribution yet, unlike tropical terrestrial counterparts, have nowhere to hide from the sun, storms, and predators. They live on the surface, surrounded by a 3 per cent salt solution, yet maintain their blood salts levels at a lower osmotic pressure than that of seawater (hypotonic) and manage to find mates in the vastness of the ocean. They live in what, to them, must be an unbounded two-dimensional world in which they are almost solely dependent on prey falling from above or floating up from below. Furthermore, they must survive predation from above (birds) and below (fish), while keeping in touch with others of their species in order to mate and produce young, with the still further challenge of avoiding falling prey to others of the same genus that face the same existential dilemmas. They reduce their risk of predation by forming ‘flotillas’ of up to one hundred individuals. Their eggs are laid in batches on any convenient floating substrate—a shed feather, floating vegetation, plastic—and even on their conspecifics. They avoid drowning by wearing what amounts to ‘mackintosh and boots’ in the form of very small hairs (microtrichia) on their legs and larger hairs (macrotrichia) on their bodies, which repel water and hold air. If they are submerged, they can survive for at least two hours under water and up to sixteen hours in cooler waters. They are extremely difficult to keep in captivity, so much remains to be discovered about these elusive animals.

Fascinating as they are, aquatic insects are in the minority, although that is still sizeable given the species richness compared with vertebrates, which they far outnumber. In this chapter, as well as considering the lifecycles and reproductive tactics of aquatic insects, we have seen how they avoid predation. In Chapter 6 we will see the adaptations that their terrestrial relatives have evolved in order to avoid falling victim to the depredations of insectivorous vertebrates and other invertebrates.

Chapter 6

Mimicry, crypsis, and blatant advertising

Insects are food for many animals, including other insects. Their main routes to avoiding being eaten are to hide, by camouflaging themselves so that they merge into the background or pretending to be something dangerous or poisonous; or to run or fly away. Several insects mimic inanimate objects, while others take on the appearance of a dangerous animal; eyespots on butterfly wings for example, are thought to mimic the eyes of vertebrate predators. Some flies and moths are incredible mimics; how many people have thought that the harmless hoverfly is a wasp or a bee, or that the clearwing hornet moth is a hornet?

Mimicry of ‘dangerous’ beasts has arisen from the practice adopted by a number of insect species that advertise their lethality by warning colours—red and black or yellow and black. Caterpillars that sequester toxins from their host plants advertise this with stripes, warning experienced bird and mammal predators that eating them will result in dire consequences. In some species the toxic effects are passed on to the adult stage, which also has warning colouration although not necessarily the same colouration as the larva. The cinnabar moth has yellow and black stripes as a caterpillar but is black and red as an adult, both colour schemes being well-known danger signs in the natural world. Presumably the change in colour from larva to adult implies that the adults have a different suite of predators to avoid.

The English naturalist Henry Bates and the German entomologist Johann Müller worked independently in Brazilian rainforests in the late 19th century, observing and collecting Heliconiid butterflies. So influential was this work that their names have been immortalized by being attached to their respective concepts. Batesian mimicry or signal, protective, or defensive mimicry, is formally defined as mimicry in which a harmless species has evolved to imitate the warning signals of a harmful species directed at a predator of them both (Figure 21). Müllerian mimicry (aposematism) or cue mimicry is defined as that in which two or more often distasteful species, which may or may not be closely related and share one or more common predators, have come to mimic each other’s honest warning signals, to their mutual benefit (Figure 22).

21. A plate from Bates’s original article, illustrating Batesian mimicry between Dismorphia species (top row and third row) and various Ithomiini (Nymphalidae) (second and bottom rows). A non-Batesian species, Pseudopieris nehemia, is top centre.

22. Müllerian mimicry in butterflies, showing four forms of H. numata; two forms of H. melpomene; and, in the bottom row, the two corresponding mimicking forms of H. erato.

Although Batesian and Müllerian mimicry has long been associated with tropical butterfly species, recent work has revealed that a mimetic complex of red and black Hemiptera, providing defence against insectivorous birds, is present in Central Europe.

Camouflage, advertising, and shock tactics

Mimicry is not all Batesian and Müllerian; other forms of mimicry are also recognized. Insects can masquerade as physical objects, so for example many Lepidoptera appear to be dead leaves, twigs, or even buds, such as the buff-tip (Phalera bucephala), and the very familiar stick insects and leaf insects that do a remarkable job of mimicking vegetation. The moth Uropyia meticulodina is almost indistinguishable from the real thing when at rest and masquerading as a dead leaf (Figure 23).

23. Adult Uropyia meticulodina masquerading as a dead leaf.

An example of cue and masquerade mimicry is seen in moth larvae and adults that appear to be bird droppings on leaves, presenting an unpalatable sight to potential predators. An example of aggressive cue mimicry is that of predatory insects that prey on spiders. The Australian assassin bug, Stenolemus bituberus, climbs on to a spider’s web and strums the threads to attract the spider towards it. Once it arrives, the bug quickly stabs the spider with its piercing mouthparts and holds it in place with its front legs while sucking out the body fluids. Conversely, an example of aggressive signal mimicry is that shown by the large blue butterfly (Phengaris arion, formerly Maculinea arion), which overwinters as a fourth-instar larva in the nests of the ant Myrmica sabuleti. In the first three larval (caterpillar) stages, the butterfly feeds on plants, and when it has finished feeding it falls to the ground, mimics the sound of an ant larva, and as a finishing touch mimics the skin chemistry of the ant larva too, fooling passing adult ants into taking it into their nest, where the butterfly larva becomes carnivorous and feeds on the ant brood throughout the winter. In the spring, the fully developed larva forms a pupa (chrysalis), chrysalis, emerges a few days later as an adult, and makes its way to the surface where it inflates its wings, seeks a mate, and lays eggs in a suitable habitat.

Depending on its orientation, the eyed hawkmoth (Smerinthus ocellata) can be thought to be masquerading as dead leaves, a bracket fungus, or even a fox. There is even a caterpillar of a moth species found in the Ecuadorian jungle that looks like a bird feather—when it moves it appears to be blowing in the wind.

Another example of impressive mimicry is the peacock butterfly (Aglais io). When its wings are fully open, its body is the same shape and colour as a bird’s beak. Even the ‘eyes’ are in the right position and with only a bit of imagination you can see a resemblance to an owl’s head. When the wings are closed, the colouration of the undersides resembles a dead leaf or tree bark; when disturbed, it opens its wings and hopefully startles the predator(s) away.

Christer Wiklund and colleagues at the University of Stockholm, Sweden, carried out some fascinating research with three leaf-mimicking butterfly species, the comma (Polygonia c-album), the small tortoiseshell (Aglais urticae), and the peacock. The butterflies were put in a large cage with some blue tits. The comma, which is the most realistic leaf mimic, was the last to be discovered by the blue tits, but as this butterfly lacks the wing opening ‘startle’ defence almost 75 per cent of this species were eaten. The small tortoiseshell butterflies, as an intermediate between the comma and peacock in terms of behaviour and mimicry, suffered 90 per cent mortality. The peacock, on the other hand, had 100 per cent survival.

Not all insects pretend to be something else; some have adopted protective colouration. Many adult insects blend perfectly into their backgrounds: the Central and South American lichen katydid (Markia hystrix) is gloriously green when freshly emerged, and the marvellously named merveille du jour (Griposia aprilina) is almost invisible when resting on a lichen-covered tree. The peppered moth (Biston betularia), which has different coloured forms or types, rests during the day as an adult on the trunks of trees that are similarly coloured. When air pollution was at its height, natural selection favoured adult moths that were darker in colour; this melanic form is now not as common in the UK since the Clean Air Act (1956) reduced the amount of soot in the air. The larvae are also cryptic (hiding in plain view), mimicking twigs, and recent research has shown that they can sense the colour of the twig that they are on and adjust their body colour accordingly.

It is not just during their active stages that insects need protection from natural enemies: this is also necessary for the eggs and pupae. Insect eggs vary greatly in colour, size, shape, and sculpturing. Some of this variation is very clearly defensive in function: spicules (spines), distasteful coating, and high levels of toxic chemicals. A less metabolically costly option is camouflage or mimicry. Eggs of the Indian stick insect resemble plant seeds, even having a fake elaiosome—on real seeds, a fleshy lipid-containing structure that encourages ants to carry and disperse them. It has been suggested that eggs of the map butterfly, Araschnia levana, mimic the flowers of its larval host plant, nettle (Urtica spp.) (Figure 24).

24. The map butterfly, the plant that is the mimic model for the eggs and the eggs of the butterfly.

Another butterfly, Agathymus estelleae, lays beige or green eggs. The former are cryptic if they fall to the ground, the latter are cryptic on the host plants, ensuring that at least some of the eggs are protected, however careless the mother might be in depositing her eggs. We may not think of ants and bees as needing to hide, but despite their stings and bites, they do have enemies. Ants are probably the largest group of social insects that use camouflage; those species that live on tree bark, soil, and rock tend to be uniformly black, brown, or grey coloured, matching their backgrounds. We can also see variation within species, in bumblebees, for example, with those that live in dry grasslands being paler than those of the same species that live in lusher, more shaded environments.

Distractive/disruptive marking

Distractive or disruptive marking breaks up body edges and creates false boundaries, which confuse predators in search of a juicy meal. Eggs of the lappet moth (Gastropacha quercifolia), the adults of which resemble a bundle of dried-up oak leaves (hence the name), have eggs that are very distinctly marked and very obvious, at least to humans, and it has been suggested that this is an example of disruptive marking (Figure 25).

25. Gastropacha quercifolia eggs.

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Insects that depend on chemical defence, which they gain by sequestering toxins from their host plants, such as the cinnabar moth that feeds on ragwort, Senecio jacobaea, make sure that they stand out from the crowd by adopting bold colouration; in the case of the cinnabar moth, as we noted earlier, the adults are red and black, and the caterpillars are striped yellow and black. The monarch butterfly (Danaus plexippus), which feeds on milkweed, a plant rich in cardiac glycosides, has very bright larvae, striped yellow and black, and the adults are a very distinctive orange and black. As with the cinnabar moth, this suggests that the predators attacking the different life stages are not the same. Once a predator, usually a vertebrate, has learned that these are distasteful, the rest of the population is safe from that individual. In some predator populations the response to danger signals appears to be innate, and, for now, prey and predator have reached an evolutionary truce.

Although most species that have evolved the use of red and yellow warning colours show these characteristics across their populations, with all individuals being the same colour, some species, such as the wood tiger moth (Arctia plantaginis), display colour polymorphism. The hind wings of the females range from yellow to red, while those of the males can be white, yellow, red, or black. Adults of the wood tiger have two forms of chemical defence: one is the release of a toxic fluid from the thorax, produced when attacked by birds, the other is the production of a similar, but subtly different, toxic cocktail that deters invertebrate predators—mainly ants. The fluid produced by white-winged males is nastier and smellier than that produced by the other colour morphs, which would make us think that the white forms would be the most common, if not the only colour morph. Although some populations are indeed monomorphic, in Scotland, all wood tiger moths have yellow hind wings; in other places, other colour forms dominate. It turns out that the frequency of the different colour forms is a result of the learning behaviour of the most common bird predators: in Scotland tits are the main predators, in Southern Finland, where the white morph dominates, dunnocks are the main predators. What about the red-winged forms? How is it that they survive in nature? It turns out that although they are not as distasteful as the white forms, they are visually more repugnant to birds, possibly because of an innate expectation, based on their experience of similarly coloured insects, that red signals danger. On the other hand, it could be that their anti-ant defences are more effective than in the other colour forms and that this allows them to persist in the population. A great example of natural selection in action, although one could wonder what would happen to the Scottish populations if the bird community were to suddenly change.

Although yellow, red, and black are colours that many insect predators recognize innately as danger signals, the insect warning palette is not limited to those colours alone. Some insects use other warning colours: the monkshood aphid (Delphiniobium junackianum) is a vivid blue, and feeds in a dispersed, but obvious, crowd, on the leaves of its very poisonous host plant, monkshood. The blue pigment is derived from the aconite that the aphid sequesters from its host plant, making it a less than tasty mouthful for any predator that chooses to ignore its warning signals.

Although adult Lepidoptera have a number of predator avoidance mechanisms—mimicry, aposematism, unpalatability, or innate behaviours—there are no peer-reviewed published references to them being able to ‘remember’ being attacked and to avoid an area for some time afterwards. On the other hand, there are many examples of predators learning to avoid distasteful lepidopteran prey. Remembering to avoid predator-rich areas would seem to be a ‘sensible’ trait to evolve, so it is surprising that the existence of this phenomenon has not yet been tested, especially as other insect groups, aphids and thrips being notable examples, have been shown to avoid plants that ladybirds and predatory bugs have previously investigated.

Having seen how good insects are at avoiding death from the actions of other animals, Chapter 7 examines how insects cope with the dangers facing them from the equally taxing effects of weather and climate.

Chapter 7

Against the odds

In addition to the risk of being eaten, insects face several environmental challenges, weather and climate being the two most obvious. Imagine having to spend winters naked on the snow-covered prairies of North America or the summers naked roaming the deserts of North Africa. This is the situation in which many insects find themselves. The problems are particularly marked in insects that live in seasonal environments, or those where there are very marked differences between night and day temperatures. Insects that live in temperate or subarctic environments need to find some means to survive the winter, be that a safe overwintering site, a change in behaviour, a physiological change, or, in many cases, all three. The main challenge is to avoid dying from the cold. The solution to this is to overwinter as a cold-hardy stage, which in insects can be any part of their lifecycle—egg, larva, pupa, adult—even in the case of organisms as seemingly fragile as moths and butterflies.

The secret lies in the anti-freeze that insects produce as winter approaches. Insects that overwinter use a mixture of alcohols and proteins to prevent freezing, in some cases (aphid eggs, for example) allowing them to survive prolonged exposure to temperatures as low as −40oC, a much-needed level of protection in a Scandinavian winter. Just because an insect can be found frozen within soil or water does not mean that it is, unlike us, freeze-tolerant (able to survive the formation of ice crystals in its body tissues); it may or may not be. If the latter, it has avoided freezing by the process known as supercooling, the ability to remain unfrozen below its melting point. The supercooling point is the temperature at which spontaneous freezing occurs in a supercooled liquid. You may have put a glass of water into your freezer and removed it some hours later to find it still liquid, but on poking a finger into it find that it suddenly solidifies, as crystallization begins when even a small speck of dust is introduced: an excellent and very satisfying example of supercooling. Purified water does not contain the impurities on which ice crystals can form. The more anti-freeze present, the lower the temperature at which an insect can supercool. Producing anti-freeze is metabolically expensive so it is in the interest of the insect to produce it only when it is needed—not all year around, but only as winter approaches. In the early days, research on insect overwintering was done largely by insect physiologists, who concentrated on the remarkable supercooling ability of insects, often as low as −20oC in some adult insects and −40oC in some eggs. Even soft-bodied insects such as aphids were shown to have supercooling points well below −10oC. This was, however, at odds with what could be seen in nature. For example, work with the grain aphid (Sitobion avenae) showed clearly that populations in the north of England, although initially increasing during early winter, died out before spring, despite the temperature not falling below −8oC. The answer lay in the method by which supercooling points were determined. The tested aphids were placed in small chambers, the temperature was lowered by fractions of degrees, stopped, and raised back to ambient levels to check whether the aphids were still alive. The temperature at which they died was recorded as the lethal limit. The researchers did not, however, check whether normal function was restored after the treatment. As it transpired, the aphids suffered cryo-injury at temperatures as high as 5oC if exposed to it for a prolonged period of time: they may well have been alive at this temperature when observed in experimental conditions, but in the field their reproduction and survival were impaired, leading to population collapse.

Overwintering strategies are not all based on internal chemistry. Another way to survive winter is to change behaviour. Many insects that normally avoid each other, except when they want to mate, become much more tolerant of each other and form large aggregations in protected sites: under the bark of trees or, as often reported by the media, in people’s houses. We have already noted earlier that in insects like ladybirds, such behavioural change is mediated by aggregation pheromones and a positive response to touch, thigmotaxis. In insects that would normally spend the winter in caves or tree hollows, there may also be a negative response to light.

How do insects know that winter is approaching? There are two cues for this: change in day length—days become shorter and nights longer once the summer solstice has passed—and mean temperatures begin to decrease. The latter is not as reliable a cue as the former so most insects depend mainly on the length of the day (photophase) or night (scotophase), as these are entirely predictable and do not vary from year to year. Each insect species has a critical phase. In the vetch aphid (Megoura vicia), the threshold is reached when night-time exceeds ten hours, whereas in the parasitic wasp Cotesia (Apanteles rubecula), the stimulus to begin diapause (a condition in which development and metabolism is greatly reduced) is when day length falls below sixteen hours. The next ‘decision’ that an insect must make is where to overwinter.

As ‘naked’ organisms, insects need somewhere sheltered and preferably well insulated to pass the winter. Soil is a remarkably good insulator; the surface temperature might be −12oC but the temperature at 160 cm depth can be as high as 6oC. This would seem to be the ideal situation, especially if there is deep snow cover, which acts as a further insulating layer. In Canada, for example, where deep snow is common in winter, the cabbage root fly (Delia radicum) is able to survive at a lower air temperature than those in the UK, where snow is much rarer. Overwintering at depth in the soil may be fine for a hard-bodied adult beetle but imagine a soft-bodied larva first digging its way down to that depth, then emerging as a delicate winged adult in the spring and having to scramble to the surface; they would suffer irreparable damage on the way. Another problem would be knowing when spring has come. In practice, most insects that overwinter in soil tend to be no further down than c.15 cm. Some insects, such as the weevil Strophosoma melanogrammum, which overwinters as an active adult stage, move between the soil and the surface, depending on the temperature, feeding on evergreen plants during warmer spells and retreating to the relatively warm subsoil environment when temperatures dip below 0oC. This brings us neatly on to the problem of which lifecycle stage to pass the winter in. Insects exist as eggs, larvae, and adults, and, if they are holometabolic, they also have pre-pupal and pupal stages. Taking butterflies and moths as an example of holometabolic insects, in a region where winters are noted for their harshness, for instance Finland, where winter air temperatures are commonly below −20oC, most species would be expected to overwinter as immobile cold-hardy stages—egg or pupa. In fact, all stages of the lepidopteran lifecycle can occur during the winter, albeit that egg and pupa are the preferred overwintering stages. It may be risky to overwinter as a fragile larva or adult but there are also advantages, not least that of being ahead of your competitors. If the overwintering stage is a pupa, insects have to emerge, mate, and lay eggs; if they are already adult, they are ready to lay eggs and exploit the newly flushing tissue before their rivals have emerged from their overwintering pupa. If they are larvae that have survived the winter, they are already in a position to begin feeding. A substantial proportion of species overwinter at more than one stage to ‘hedge their bets’.

Of course, it is important to know when spring has arrived. Insects use increasing temperatures and increasing day lengths to know when to emerge from diapause, although some species, such as the pine beauty moth (Panolis flammea) and the cabbage root fly, also have to have been subjected to a period of subdevelopmental temperatures before they will respond to the spring cues, somewhat similar to the vernalization process in plants.

At the other end of the scale is extreme heat and drought. In this case, anti-freeze is not an option although tropical insects still have the ability to produce cryoprotectants. There are two aspects to this part of the insect story: insects that are desert dwellers and must cope with extreme conditions throughout their lives, and insects that only experience extreme heat and drought occasionally; the former are well adapted to the conditions, the latter less so.

Behavioural and physiological responses are the key to desert survival. Insects that are desert-adapted have special modifications compared with their temperate and tropical relatives; there are morphological, physiological, anatomical, and behavioural adaptations. Desert insects tend to be quite large, reducing relative surface area and preventing undue water loss. Unlike insects that live in dry non-desert conditions, the legs of desert insects are usually long to avoid contact with the hot desert surface, and they often have a sub-elytral cavity, again to reduce water loss. Physiologically, desert insects have three main forms of defence. They can tolerate low water content of their haemolymph: essentially, they have thick blood. Like other animals that live in dry conditions, they retain as much water as possible in their secretory processes. Insect frass (droppings) is generally dry but in desert insects it is exceptionally so; every molecule of water is precious. They exhibit discontinuous ventilation (cyclical breathing), which can be thought of as the insect holding its breath. The spiracles (Chapter 1) are kept closed for most of the time but as oxygen is used and carbon dioxide (CO₂) accumulates in the haemolymph, it is held in solution mainly in the form of bicarbonate. As CO₂ levels build up, the spiracles open slightly, allowing some oxygen to enter and a little of the CO₂ to escape. Finally, as the level of CO₂ reaches a critical threshold, the spiracles open completely and the carbon dioxide is released in one big burst.

Other desert insects take advantage of the occasional mists or fogs and drink water from where it accumulates on bits of detritus. Some tenebrionid beetles construct troughs and mini sand dunes to collect their own water. Other tenebrionid beetles have anatomical adaptations to do the same job. The darkling beetle (Stenocara gracilipes), and related species, intrepid inhabitants of the Namib Desert, represent probably the most well-known examples of extreme desert adaptation. Their long legs reduce contact with the hot sand, and their cuticle, composed of hydrophilic and hydrophobic grooves and bumps, channels water harvested from the morning sea fogs to their waiting mouths (Figure 26). Other desert-dwelling insects are largely nocturnal, spending the day beneath the soil surface or under convenient stones or similar sites.

26. The darkling beetle, Stenocara gracilipes.

Drought, which may, if current predictions for climate change are correct, become an ever more frequent event worldwide, is likely to cause insects in temperate regions many more problems than those faced by the desert dwellers. Drought in temperate and tropical regions is usually paired with high temperatures. In tropical regions this is not such a big problem because tropical insects have higher thermal limits than temperate insects. Although, in general, higher temperatures allow insects to complete their lifecycles more quickly, there are thermal tolerances to be considered. The temperate species known as the alfalfa aphid (Acyrthosiphon kondoi) has an optimum temperature limit of c.15oC while the tropical aphid Aphis gossypii does best at about 25oC, a temperature that the former species finds hard to tolerate for any length of time. Drought can affect all stages of the insect lifecycle—egg hatch, larval feeding and development, adult and larval behaviour, fecundity, and oviposition.

The eggs of many beetle species need to absorb water before they can hatch; those of the Western corn rootworm (Diabrotica virgifera) desiccate at low humidity, while in other species, egg hatch and survival are much reduced under drought conditions. Insects with soil-dwelling larvae are particularly susceptible to drought—young leather jackets (larval craneflies) are very dependent on moist soil for survival, as are larvae of the weevil Sitona hispidulus. The depth at which larvae of the click beetle (Agriotes lineatus) feed and their abundance are affected greatly by rainfall; low soil moisture results in reduced abundance. Oviposition of the southern mole cricket, Scapteriscus borellii, is greatly delayed once soil moisture falls below 10 per cent.

Drought in areas where it is not a regular occurrence can have marked effects on insect populations, either directly or, in the case of herbivorous insects, through the impacts on their host plants. In the UK and USA, for example, highly mobile butterfly and moth species with southern distributions tend to increase in abundance after drought periods whereas less-mobile species with northern distributions show population decreases. Herbivorous insects are not the only insects that are affected by drought. Carabid beetles, many of which are predatory, were also affected by the UK droughts of the mid-1990s; species that were adapted to damp and moist habitats and low temperatures showed significant decreases in abundance. Insects and plants have a complex relationship when it comes to drought stress.

In 1969, an Australian entomologist, Tom White, came up with an alluring hypothesis to explain insect outbreaks, one which dominated the field for at least twenty years and is still being tested. This was the famous, perhaps infamous, plant-stress hypothesis. White noticed that outbreaks of the psyllid, Cardiaspina densitexta, or as the Australians call it, the Eucalyptus lerp, were associated with drought or waterlogging. He hypothesized that trees were undergoing stress, which made the soluble nitrogen content of the foliage more accessible to the insects, enabling them to develop into larger, more fecund adults, ultimately leading to the outbreaks. A few years later, an American entomologist, Doug Rhoades, supported this hypothesis but added that the defences of the stressed trees were also impaired so that, as well as having a more nutritious food source, the insects had more resource available for reproduction as fewer were being diverted to overcoming the plant defences. This hypothesis resonated with entomologists and ecologists who, understandably, saw it in human terms of susceptibility to illness when stressed.

While field observations seemed to support the hypothesis, experimental evidence was and remains harder to come by. Herbivorous insects do not all feed on plants in the same way; some have much more intimate relationships with the plants than others. Sap-feeders exploit the phloem or xylem; defoliators strip the leaves; then there are shoot or stem borers, leaf-miners that live within the leaves feeding on the internal tissues, and gallers that manipulate plant tissue by the ‘injection’ of salivary compounds. It would seem obvious that insects with different feeding modes may not respond to stressed plants in the same way. A couple of influential reviews in the 1990s suggested, however, that experimental studies gave very different results from field observations. When researchers looked at outbreaks in the field they were apparently more likely to see the effects of plant stress than under experimental conditions, probably due to the fact that the conditions that supposedly induced plant stress, i.e. hot weather, also enable insects to grow quickly, develop faster, and be more fecund. Experiments under controlled conditions were much more ambiguous and related to the feeding mode of the insect. A meta-analysis in 2004, by Susan Huberty and Bob Denno, showed that phloem-feeders such as aphids performed worse on drought-stressed plants, while leaf chewers seemed unaffected.

The way in which the plants are stressed may influence the outcomes for the insects. Joanna Staley conducted an interesting set of experiments at Wytham Woods, near Oxford, UK. She subjected experimental plots to two treatments, a complete summer drought and a wet summer, with 120 per cent of normal rainfall, and studied lepidopteran and dipteran leaf-miners on different host plants. She found that some responded positively to stress while others did not, so there was no consistent response to plant stress within that feeding guild. Similarly, experiments with aphids showed differing responses depending on species and stress type—responses that were not in direct proportion to increasing drought. In nature however, drought or waterlogging is not always continuous; dry spells can be interrupted by wet spells. This leads to the pulsed stress hypothesis. To test this, we did experiments using spruce aphids on conifers subjected to a variety of treatments ranging from continuous drought, waterlogging, and intermittent rain and drought. We found that intermittent, pulsed drought stress benefited the aphids, whereas long spells of drought and waterlogging had detrimental effects on them. Ladybird predators, on the other hand, increased their aphid consumption rates when drought was prolonged but ate fewer when drought conditions were intermittent. Aphid parasitoids also show similar interactions. These experiments reveal how complex the interactions between plants, their stress effects, and insect herbivores can be, especially when natural enemies are factored in.

In summary, whereas insects are well adapted to predictable occurrences of cold and extreme heat, the direct effects of drought can cause changes in the timing of insect development, their survival, and abundance. All stages of the lifecycle can be affected. Indirect effects, those brought about by the host plant, may be non-linear, and are inconsistent across feeding guilds and orders. Much more work needs to be done if we are to understand the effects of climate change on insect populations.

Chapter 8

The good, the bad, and the ugly

Most people think of insects as good or bad, honeybees and other pollinators versus mosquitoes and crop pests, like the ubiquitous greenfly, and that, in a nutshell, is the problem. Insects are not just pests and pollinators. Most insects do not harm humans; a very small percentage of the known one million plus species have shaped our viewpoint of these fascinating and useful animals.

Leaving aside the cultural influences, human existence depends on insects. Pollinators are important, but these are not just honeybees; flies, beetles, moths, butterflies, wild bees, and other Hymenoptera play their part in making sure that our food crops are fruitful. There are also the largely unseen, overlooked insects busy helping with the recycling processes, improving soil quality, and acting to reduce the numbers of insects that would, unchecked, threaten our very existence. It is indisputable that without modern crop protection, we would lose maybe half of our crops during growth and storage, but to a certain extent that is our fault for providing such tempting delicacies for the less than 5 per cent of insect species that share our tastes.

As well as insects that provide us directly with food and other products, honey, wax, food colourings, and protein, we have harnessed the specialist killing behaviour of many insect predators and parasites and used them to provide us with residue-free food and hopefully sustainable agricultural systems. We still have much to learn in this area.

Insects as pests

As mentioned previously (Chapter 3), most insects are herbivorous. Insects that make a living from the same plants that feed our livestock and ourselves are thus in direct competition with us and regarded as pests. Modern agriculture and the overuse of synthetic pesticides are often cited as the cause of all our pest problems; that is far too simplistic. We only need to read the Bible to hear of plagues of locusts, or look closely at the Bayeux Tapestry to see a bird scarer in action, or read accounts of popes and bishops in medieval Europe excommunicating crop pests, to realize that pests and diseases have existed since humans stopped being hunter-gatherers and became farmers. Modern agriculture has not caused pest problems, although it has undoubtedly exacerbated the situation; the problems date back to those first humans who selected the seeds of the tastier, higher yielding plants that they first cultivated. The characteristics that they selected for—sweeter, more succulent, larger grains/fruit—meant that the plants were less well defended against their herbivores, including us, and thus more susceptible to attack by both specialist and generalist insect species. The things that are unpalatable to us are unpalatable to the insects that feed on those plants; by making plants more human friendly, we have also made them more attractive to the insects that prey upon them.

A long-held premise for why insects can be pests is that pest outbreaks tend to be associated with pure monocultures of crops. The hypothesis is that natural enemies were more abundant and effective in vegetationally diverse areas than in monocultures, the so-called ‘enemies hypothesis’. This idea has been around a surprisingly long time; in 1947 the South African entomologist George Ullyett remarked, ‘where weeds occur around headlands and in hedges, they should be left for the purpose of supporting parasites and predators important in the natural control of the diamond-back moth (Plutella maculipennis Curt)’. A decade later, Charles Elton referred to this statement, explaining that ‘these hedgerows form a reservoir for enemies and parasites of insects and mite pests of crops’.

Richard Root, an American ecologist, explained the premise of the ‘enemies hypothesis’ as follows. Predators and parasites are more effective at controlling herbivore populations in diverse habitats or plant communities because diverse plant communities support a variety of herbivores appearing in different seasons, providing a steady supply of prey for the predators. In addition, complex environments provide refuges for prey, thus allowing the prey not to be completely eradicated. Diverse plant communities also provide a broad range of additional resources, such as pollen and nectar, for adult natural enemies.

Root ran his experiment for three years and did indeed find a significant difference in herbivore load between the pure plots and the weedy rows, the former having a greater abundance of pests (mainly aphids and flea beetles) than the latter (Figure 27).

27. Difference in herbivore load between the simple plots and the weedy rows.

He did not, however, find any difference in the numbers of natural enemies between the two treatments. He thus had to come up with another idea to explain his results. His ingenious explanation is encapsulated in what he called the resource concentration hypothesis, which states that herbivores are more likely to find and stay on hosts growing in dense or simple stands or monocultures, and that the most specialized species often reach higher relative densities in simple environments.

Root hypothesized that specialist herbivores were ‘trapped’ on the crop and accumulated while more generalist herbivores were able and likely to move away from the crops to other host plants. He added that the ‘trapping effect’ of host patches depends on several factors, including stand size and simplicity. His colleague Jarmo Tahvanainen developed two new hypotheses to explain why more diverse cropping systems have fewer pest problems than monocultures, one of which he termed associational resistance. He proposed that plants growing in a complex, mixed community offer an ‘associational resistance’ to herbivores beyond that of the individual plant species, which is lost in monoculture cultivation, allowing specialist herbivores to proliferate.

In the Chemical Interference Hypothesis, he postulated that reduced herbivory in diverse communities is due to chemical stimuli produced by non-host plants interfering with host finding or feeding behaviour of specialist herbivores. In simple terms, a monoculture sends out a very strong signal, which could be olfactory, for example a strong bouquet of crucifer volatiles; for other herbivores it could be visual, or a combination of the two. Intercropping increases crop diversity and changes the crop ‘signal’ to one that now ‘confuses’ the specialists (Figure 28).

28. Cropping systems: (a) Conventional intensive agricultural landscape sending out strong ‘signals’ to specialist herbivores; (b) the intercrop melange effect—sending confusing signals.

The message from the many studies on the effect of intercropping crop diversification on pest abundance is that, in general, polyculture is beneficial in terms of promoting biological control, and that incorporating legumes into the system gives the best yield outcomes.

Another form of intercropping that overcomes the potential problems of harvesting different crops from the same field is the concept of planting different genetic variants (genotypes) of the same species. Resistant plants tend to have fewer generalists present, although their individual yield may be reduced. By planting a mixture of susceptible and resistant genotypes, it is possible to have your cake and eat it, especially if it is not essential to have a single genotype crop. This approach has been used to good effect in the production of short-rotation willow coppice, where planting diverse genotypes of the same species reduces both pest and disease levels.

Insects as vectors of disease

As well as the damage that insect herbivores cause directly to crops, they can also be very efficient vectors of disease to crops, livestock, and people. Insects with piercing and sucking mouthparts feeding on plant sap or vertebrate blood need to inject an anti-coagulatory agent, which they do via their salivary glands. A number of viruses and other micro-organisms have taken advantage of this and are transmitted from their insect host to their plant or vertebrate host where they multiply and cause harm to the host. Aphids, for example, carry and spread a number of deadly plant viruses, some in a passive way, akin to disease transmission via a contaminated hypodermic needle. In other interactions, the virus multiplies in the body of the insect host. Mosquitoes and other stinging and biting flies transmit viruses and protozoan diseases to vertebrates including humans. The virus that causes blue tongue disease in domestic livestock is transmitted by biting midges; the protozoan disease malaria is transmitted by mosquitoes; Leishmaniasis, another protozoan disease, is transmitted by sandflies. These and the plant viruses are the result of coevolution between the disease-causing organisms and their intermediate hosts, many of which have resulted in behavioural modifications which improve disease transmission. Other diseases, such as those caused by bacterial infections, although no less harmful, are a result of the feeding habits of insects such as houseflies and ants, and are accidental rather than deliberate.

Biological control

Although most insects are herbivorous, 25 per cent make a living at the top of the insect food chain—the predators and parasitoids. Most people are aware of the almost ubiquitous spotted red and black ladybird beetles and their voracious appetite for aphids; some are discomfited when they encounter a spider going about its business; few realize that there are many more hunters and killers roaming their gardens and hedge bottoms. Although predators such as these are important in keeping pest insect populations low, they are, arguably, not as efficient as the parasitic insects that carry out their activities largely unseen by humans.

Predators, parasites, and parasitoids

As with herbivorous insects (Chapter 3), insect predators have to locate their prey. Some insects such as dragonflies, carabid beetles, and ladybirds are predators as larvae and adults; others like hoverflies, only as larvae. Many larval predators, especially those that feed on herbivorous insects, are already in the vicinity of their prey, having been deposited there as eggs, so they do not have far to travel. How do the adults, either as predators themselves or as mothers needing to find a suitable home for their offspring, know where their prey are? Generalist predators, such as carabid and rove beetles, are mainly ground-dwelling and roam the soil surface, feasting on foliage-feeding insects that have fallen from above (about 15 per cent of cereal aphids find themselves on the ground) or hunting down the soil and subsurface organisms, Collembola, slugs, snails, etc. Insects with more specialist needs, such as ladybirds and hoverflies, that feed mainly on aphids, use chemical and visual cues to locate their prey; they look for plants, signs of aphid feeding, sticky honeydew, and respond to the ‘scent’ of their prey. Adult ladybirds and hoverflies seem to be able to judge whether an aphid infestation is growing and will lay their eggs near flourishing colonies rather than near declining colonies. This may be due to the fact that foraging aphid-eating predators leave behind oviposition-deterring and foraging pheromones. Interestingly, some aphid species also seem to be able to detect these volatile signals and avoid landing on those host plants.

Plants themselves also help natural enemies to detect their prey. When attacked by herbivores, plants produce the equivalent of an immune response. Distasteful chemicals move rapidly to the site of the injury, encouraging the herbivore to move elsewhere to feed. They therefore cause the insects to make more holes, effectively advertising their presence to potential predators. Simultaneously, the plant sends out chemical signals telling insect predators and parasites that there is a meal or host available. Parasitoids, which live at the expense of their host organism, causing it to die, are particularly adept at recognizing plant volatiles. Some parasitoid species use the smell of the host plant of their favourite prey as the initial signal, then search the plant for their insect host. This close association between parasitoid-searching behaviour and host plant can have unexpected consequences. In the UK in the 1970s the native pine beauty moth Panolis flammea became a serious pest of lodgepole pine, Pinus contorta, which, although not as nutritious a host for the moth as the native Scots pine, Pinus sylvestris, was an enemy-free space in plantations. It transpired that the parasitoid wasps that kept the moth under control in Scots pine plantations were ‘hard-wired’ to the volatiles produced by Scots pine and did not recognize those produced by lodgepole pine. It was twenty years or more before the biotypes of parasitoids able to recognize lodgepole pine appeared in the population and the pine beauty moth problem subsided.

Before the advent of modern pesticides, farmers depended on cultural control methods like crop rotation, and direct protection against pests—scarecrows, humans with sticks and rattles, and, later, netting and other shelters. None of these methods was particularly effective and some crops were destroyed completely, resulting in famine and widespread starvation. There were many ingenious attempts to prevent crop loss from pests but it was the middle of the 19th century before a more effective method became available: this was the concept of biological control. The idea was not entirely without precedent. Charles Darwin’s grandfather, Erasmus Darwin, noticed that the cabbages in his garden, although being attacked by larvae of the cabbage white butterfly, were being protected to a certain extent by parasitic wasps. He noted that this might be of use to gardeners. We know that before and up to the late 19th century, Chinese citrus growers introduced ant nests to their orchards and tied bamboo poles between trees to encourage the ants to forage more widely and reduce the number of pests feeding in their trees. Bedouins were also known to transport ant nests to oases in the desert where date palms were grown.

It was not until the 1870s that Charles Riley, a British entomologist employed by the United States Department of Agriculture, and regarded by many as the father of biological control, began to adopt a scientific approach to the biological control of pests. The first attempt was against the plum weevil, which was causing devastation to orchards in Missouri. Riley introduced natural enemies from other parts of the United States to the affected orchards. Although some control was achieved, it was insufficient to promote widespread adoption of the technique. In the 1880s the Australian native cottony cushion scale (Icerya purchasi) arrived in the newly established, highly profitable Californian citrus industry. The scale rampaged through the orchards and, despite the best efforts of the growers, who even resorted to using hydrogen cyanide gas, was unstoppable and threatened the very existence of the industry. Many growers burnt their trees, sold their land at greatly reduced prices, and left the state.

In 1888, Charles Riley sent Albert Koebele to Australia to look for natural enemies of the scale. Koebele returned with a ladybird beetle, the Vedalia beetle (Novius (Rodolia) cardinalis), which was then reared under controlled conditions and released into the orchards. Together with a parasitic fly, this approach eradicated the scale almost completely within a few years and allowed the citrus industry to develop successfully. This was the birth of what is now known as classical biological control and heralded a huge number of introductions, some of which were very successful, others much less so. Riley also recognized that parasites and parasitoids were likely to be much better biological control agents than predators. Unfortunately, with the arrival of efficient, modern synthetic organochlorine pesticides in the late 1920s, biological control was put on the back burner for a number of years.

Despite its relatively long history, the term ‘biological control’ was not coined until the 1960s, by Paul DeBach, an eminent proponent of the approach (Figure 29).

29. Biological control in theory. The introduction of the natural enemy reduces the damage caused by the pest to below the economic injury level.

Biological control has been used in glasshouse crops for more than sixty years, and in organic agriculture. More recently, because of public concerns about the environment and the overuse of pesticides, coupled with the rise in the number of pest insects showing insecticide resistance, biological control and integrated pest management have moved up the agenda again. Biological control is a complicated process, and now encompasses a variety of approaches, some of which bring with them ethical issues, especially when introducing non-native agents.

The possible non-target effects have to be studied carefully, which can take several years of trials. If these are overlooked, unintended consequences can occur. The harlequin ladybird (Harmonia axyridis), a very effective predator of aphids, is also not averse to eating other ladybirds (intra-guild predation) and has been implicated in a drastic reduction in the number of native ladybird species in mainland Europe and in the UK, to which it was unintentionally introduced. Although predators were, and still are, the first choice of many biological control programmes, parasitoids are an increasingly common option, the degree of host specificity and ability to reproduce parthenogenetically being huge advantages when compared with predators.

Parasitoids

Parasitoids prey on other insects. They differ from parasites in that they kill their hosts, and from predators in that their victims are not killed immediately. Parasitoids lay their eggs in or on their hosts. Most parasitoids are Hymenoptera but examples are found among the Diptera, Coleoptera, and Strepsiptera.

They are divided into two types.

The Idiobionts, typically living on the host’s body (they are ectoparasites), prey on adult or late-instar insects. They immobilize their hosts, so that no further development occurs, and then kill them. They have a broad host range and their hosts are found in concealed locations. Idiobionts do not have to adapt to the host’s immune system but lay eggs in inaccessible places on the host and also prevent haemolymph clotting to make it easier for the larvae to feed.

The Koinobionts are typically endoparasites that do not kill their hosts after oviposition, allowing further development. They forage in exposed situations, and are specialist, sometimes genus specific. They lay their eggs in areas where immune response may not operate and in some cases the eggs and larvae show molecular mimicry. Koinobionts parasitize young insects, as they need to allow them to grow.

Both use similar host location mechanisms, volatiles, and visual clues and some Diptera use phonotactic clues.

Such issues aside, there are a number of advantages of using biological control instead of conventional pesticides. A biological control agent is extremely selective; it only attacks the target organism, and is itself able to find the target rather than having to be delivered via a spray machine. Once established successfully, biological control organisms can propagate themselves, giving lasting control, and, unlike conventional pesticides, it is highly unlikely that the pest will be able to develop a resistance to them.

There are, of course, some disadvantages, the speed of kill being one that farmers notice particularly when comparing the knock-down effects of conventional insecticides with the much slower kill rates of a biological control agent. Once they get used to seeing the pest species still in their crops but at the same time increasing their profits from reduced pesticide input, and seeing the environmental benefits that accrue, a significant minority of farmers are being converted.

Insects as ecosystem engineers

Insects fulfil many important roles within ecosystems: pollinators, saproxylics, carrion, and dung feeders.

Pollinators. Insect herbivores are able to feed on all parts of plants—leaves, stems, roots, even flowers. Flower feeders range from specialized pollen feeders, such as the aptly named rape pollen beetle (Brassicogethes (Meligethes) aeneus) to chrysomelid beetles in the genus Phyllotreta that eat petals, to the sap-feeding aphids, like those found on roses, feeding preferentially on the newly expanding flower buds. All these are loosely termed anthophilous—flower loving. Not all anthophilous animals are insects; some bats and birds are anthophilous too.

These examples of flower feeding by insects are what we might consider exploitative, and cause direct and indirect harm to the plants; pollen removal decreases fecundity while petal removal and damage reduce the chances of pollination by altering the signals sent to pollinators. On the other hand, pollinators have evolved a mutually beneficial relationship with plants. In exchange for a quick energy boost and some amino acids—nectar—mobile pollinating insects help their sedentary plant partners to spread their genes far and wide in a much more efficient way than plants dependent on the wind.

Although important pollinators, honeybees are domesticated animals and play a minor part in the pollination of flowering plants as a whole. In fact, there is growing evidence that the recent upsurge in domestic beekeeping is posing a threat to native wild pollinators by competing for resources and spreading diseases. Flies, beetles, moths, butterflies, wild bees, and the other Hymenoptera are major pollinators that are largely overlooked. Without midges pollinating cacao plants, we would not have chocolate. There are also some vertebrate pollinators but here we will only consider insects.

Unsurprisingly, pollinators and their plant partners are physiologically co-adapted to exploit their respective needs. One obvious such adaptation is the length of the mouthpart, which decides which nectar feeders pollinate which plants. The deeper the nectar is concealed within the flower, the longer the mouthpart required to reach the sugary reward, so, for example, there are both short-tongued and long-tongued bumblebees. The common garden bumblebee, Bombus hortorum, has a tongue long enough to feed from lavender flowers, a nectar source inaccessible to honeybees and short-tongued bumblebees, like Bombus terrestris. In 1862, Darwin, to the scorn of many, predicted that the Malagasy orchid, Angraecum sesquipedale, whose nectar is produced at the bottom of a 30 cm long tube, would be pollinated by a moth with a tongue long enough to reach the nectar. It was not until 1903, when Morgan’s sphinx moth (Xanthopan morganii praedicta) was discovered, that Darwin was proved right.

Blue, purple, and mauve flowers, such as those of clovers (Trifolium) and louseworts (Pedicularis), are visited more often by bees than by other insects, and are also structurally adapted to pollination by them. Some butterflies are also attracted to purple flowers like Phlox, and these are adapted to butterfly mouthparts. Night-blooming flowers tend to be heavily scented and white or pale in colour, the scent acting as the long-distance come-hither to the night-flying moths, which are their main pollinators, the contrasting white colour against the dark foliage helping them navigate into the mouth of the flower. White and yellow day-blooming flowers have exposed nectar and are visited by a multitude of short-tongued insects: hoverflies and parasitic Hymenoptera, for example.

Scent plays a large part in the pollinating process. Although insects are visually capable, albeit seeing different wavelengths from humans, their powers of odour detection are diverse and acute. Scent is a way in which some plant species can enhance their chances of finding a mate. By producing an odour that is very specific to a particular group of insects, they can ensure that their pollen is deposited in the correct place. So some plants have flowers that smell of rotting meat or dung, others have musky scents attractive to biting flies, and others, like the pipevine, Aristolochia macrophylla, mimic the smell of fungus to attract fungus-feeding flies such as phorids.

Pollen feeders pollinate yet another subset of plants, those that reward pollinators only with pollen, no nectar provided, or, as in the case of many orchids, deceptive sexual activity. That said, orchids are generally honest brokers, most providing nectar as a resource for their pollinators. About a quarter of orchid species are, however, frauds or cheats, pretending to be either a food source or a receptive female insect. The bee orchid, Ophrys apifera, for example, is pollinated by a solitary mining bee, Eucera longicornis, belonging to a group commonly known as long-horned bees. If you look at the female bee, which is what we suppose the flower is mimicking, you can just about convince yourself that there is a slight resemblance between the two (Figure 30). Of course, bear in mind that insects do not see things in the same way as humans do, so what we think is almost certainly irrelevant. That said, it doesn’t actually have to be a particularly good visual mimic for the insects either, as it is the smell that really matters, or as long as the flower is the right shape to enable the deceived male to copulate in such a way that it picks up the flower’s pollen.

30. The bee orchid, Ophrys apifera, with pollinator, Eucera longicornis.

The fly orchid, Ophrys insectifera, is also sexually deceptive but, despite its common name, is pollinated by digger wasps and bees. Some orchids are even more cunning: the scarce marsh helleborine, Epipactis veratrifolia, releases aphid alarm pheromone in order to attract its pollinators, adult hoverflies, the larvae of which feed on aphids.

Saproxylics. Wood—hard, tough, fibrous, nutritionally poor, and very well defended—is not a habitat to be exploited by the run-of-the-mill insect herbivore. Wood is composed principally of cellulose, hemi-cellulose, and lignin, with hefty doses of tannins and terpenes. Lignin, tannins, and terpenes are its major defensive components, acting as digestive enzyme blockers, poisons, and deterrents. The carbon:nitrogen ratio of wood is very high, up to 1,250:1 compared with the 4:1 to 10:1 found in other material consumed by insects. Dead wood was a much-threatened habitat until fairly recently; modern forestry practice saw dead wood as an eyesore, wasteful, dangerous to humans, a fire risk, and a possible route for disease. This opinion is still held by many managers of public parkland and green spaces, although it is no longer universal.

But a much-overlooked part of the insect community is the insects that live in or on dead and decaying wood. This is somewhat understandable as they spend most of their lives hidden from sight under the bark or in the heart of their woody substrates. Saproxylic insects are those that live on dead or dying wood, or on the fungi and other insects found upon it. The term saproxylic is relatively modern, coined by the French entomologist Roger Dajoz in 1966; over 50 per cent of forest beetle species are recognized as being saproxylic.

As organic matter decays it experiences and imposes changes in physical, chemical, and ecological conditions, including sequential changes in species composition, known in ecology as succession. Although often grouped under the general term ‘succession’, a distinction should be drawn between successions that occur on substrates that degrade and substrates that do not degrade and that culminate in relatively stable endpoints. A defining characteristic of wood colonization is that the decay process itself imposes a finite, relatively short-term time limit within which communities can develop. Wood decay ultimately comes to an end because the substrate is metabolized and mineralized in its entirety; the resource decomposes completely and returns to the soil. This form of succession—degradative succession—is very distinct from landscape-level successions that take place as bare ground is replaced by plant communities of increasing complexity over a period of decades. Degradative succession by contrast occurs over a shorter timescale ranging from months to years, and encompasses any element of dead organic matter experiencing sequential species invasions.

As wood decomposes, it is colonized by a succession of fungi and fauna. The fruiting bodies of wood-decaying fungi can themselves be colonized by successive complements of species throughout the course of their lifetime. The routes to mineralization are complex and varied, depending on tree species and, very importantly, on which fungal species is the first colonizer.

The evolution of woody tissue, like the development of flowering plants, provides a unique resource for insects. Wood is dense, providing a highly protective environment, especially for the vulnerable larval stages. On the downside, it is tough, nutrient poor, and many adaptations are needed to exploit it effectively. The insect group that has exploited it the most effectively is the beetles, most notably a number of families including the buprestids, the anobids (deathwatch beetles, woodworm), the cerambycids (longhorns), the scolytids (bark beetles), and the curculionids (weevils). In some, the adults are streamlined with bullet-shaped heads, making it easier to move through the tunnels that they chew. Insects that feed as larvae are often legless or have reduced legs. To compensate for this they are wider at the thorax than elsewhere, allowing them to anchor themselves in place as they chew through the wood. The mouthparts of the wood-feeding larvae and adults are often toothed and reinforced with metal ions, most commonly zinc. They also have to be able to digest wood. The ability to digest cellulose directly is not common; instead it is accomplished by enzymes, obtained by a symbiotic relationship with protozoans, bacteria, or fungi.

The next most common inhabitants of dead wood are the wasps. These are mainly present not as part of the decay process but as natural enemies of the wood feeders. The female wasps, like the beetle wood feeders, have specially adapted ovipositors. Wood feeders like the wood wasp, Sirex noctilio, are equipped with a metal-tipped serrated ovipositor, which, although harmless, inspires fear in many humans, who assume it to be a particularly deadly sting. Parasitoid wasps that prey on the larvae of bark and wood beetles also come equipped with long, complex ovipositors. The sabre wasp (Rhyssa persuasoria) lays its eggs in the larvae of wood wasps and longhorn beetles living inside fallen trees. The female searches likely trees, drumming with her antenna on the trunk surface, and making exploratory probes with her ovipositor, until she is satisfied that there is a host below. She then drills into the wood using her extremely long (up to 40 mm), zinc-toughened ovipositor to locate the larva and lay her egg within it.

The process of degradative succession, by which a fallen tree or bough returns to the soil, is a complex interaction between the fungi colonizing dead wood and the insects. Although the decay process can succeed without the insects, they aid and, in some cases, abet the process. The general trend is that the insects exploiting fallen trees are initially specialist with a narrow host range, seeking out particular tree species. As decomposition progresses, it is the stage of decay that becomes important, not the tree species.

Fungi and insects have enjoyed an extensive co-existence, resulting in the evolution of a diverse range of interactions. Specialization can occur at different levels: beetles, for example, that feed on bracket fungi (tree-fungus beetles or ciids) and beetles that seek out specific genera of trees. Mutually beneficial or at any rate harmless associations between insects and fungi (mutualisms and commensalisms) enable, among other things, the transportation, dispersal, and vectoring of fungal propagules. Such relationships resolve the problem of spatial discontinuity between resources. They ensure fungal transmission to new resources, inoculate fungi into otherwise inaccessible areas, and can enable cross-fertilization. The presence of insects also serves to modify the decaying wood habitat. Feeding, burrowing, and excretion can favour fungal growth by increasing the surface area available for attack, by reducing the resistance to gaseous diffusion, and by increasing the water-retaining ability of the substrate.

Bark and ambrosia beetles transport (via guts, exoskeleton, or specialized organs called mycangia) and inoculate fungi and other microbes into the wood that they colonize. Bark beetles usually colonize the inner tree bark (living and dead phloem tissues) whereas the majority of ambrosia beetles colonize the xylem (sapwood and/or heartwood) of dying or newly dead trees. Many bark and ambrosia beetles are pests capable of eliciting enormous outbreaks having severe effects on forest structure or, as in the case of Dutch elm disease, changing a whole landscape. The relationships between these two groups have various functions and differ considerably in their specificity, evolutionary history, and consistency of association. Some fungi are used as a food source—by concentrating nitrogen or by acting as a source of sterols, they become very attractive to specialist beetles like the tree-fungus beetles. Others, such as the ambrosia beetles, feed almost exclusively on the fungal symbionts that they cultivate in galleries bored into sapwood. The beetles maintain highly specific relationships with particular fungal species; their reproduction and survival often depend entirely on the fungal symbiont. Fungal associates may also augment beetle colonization, for example by attacking and/or conditioning the wood, by helping to neutralize tree defences, or by providing protection against antagonistic fungi. Fungal symbionts may also play a role in beetle chemical ecology by contributing to pheromone synthesis and/or acting as signals themselves.

Despite the rapid growth of interest in this topic over the last few decades, the study of saproxylic insects is in its infancy; much remains to be discovered.

Carrion and dung feeders (necrophagy and coprophagy). While the sight of a fallen tree returning slowly to the soil may inspire the poet and provide a mossy bench, the stench and sight of a rotting corpse or pile of dung has the opposite effect. Happily for us, there are insects that specialize in such, to us distasteful, protein sources too: the necrophages. Most necrophagous species are flies, the most obvious being the blowflies (Calliphoridae) and flesh flies (Sarcophagidae) beloved of forensic scientists; other flies are also involved, for example the so called ‘horrid phorids’, an extremely versatile group, have several species that feed on vertebrate flesh. The main beetles associated with carcasses are the silphids, of which there are two subfamilies, the burying beetles (Nicrophorinae), which, as the name suggests, bury the carcasses on which their larvae feed and develop, and the sexton beetles (Silphinae). The burying beetles colonize recently dead corpses in order to avoid competition with the fly larvae while sexton beetles colonize the carcasses later in the decomposition process, the adults feeding on the maggot masses, the larvae on the decaying remains. Both groups show parental care and cooperative behaviour (Chapter 4).

Dung beetles and dung flies (scatophagids) play a vital role in reducing animal waste products, hence the concerns regarding the use of persistent anthelmintics, drugs such as ivermectin that eliminate parasites, in farming. Not only do they kill the parasites of livestock but they remain active after passing through the animals and kill the flies and beetles that would normally remove the dung pats within weeks or, in the tropics, days, resulting in a build-up of dung in the fields.

Dung is usually an ephemeral resource and insects that rear their young on it live in a highly competitive world. Once they locate a dung pile, dung beetles roll up a ball of dung and remove it to a location away from possible ‘theft’ by other dung beetles before the female lays her eggs in it. They thus need to move in a straight line away from the dung pile, which they do by navigating by the moon or stars.

Dung beetles are surprisingly selective about what type of dung they use, as the farmers who introduced sheep and cattle to Australia discovered. Native dung beetles prefer marsupial dung, so, in order to combat the build-up of cattle and sheep dung, European dung beetles had to be introduced, yet another unintended consequence of not understanding the vital role that insects play in the world.

In the final chapter (Chapter 9), we will consider the consequences of ignoring the role of insects in ecosystem and global health, and what we can do to mitigate the damage already done to their existence.

Chapter 9

Ecological Armageddon—insects in decline?

I began by describing the diversity and ubiquity of insects. I discussed their origins and marvelled at the ways in which insects have adapted to a wide range of environments and the roles that they play in maintaining ecosystem health. It is thus fitting to end by discussing the harm that we are doing to insects and the planet that we, and they, inhabit, and ways in which we might act to halt or reverse our course, if it is not already too late. Eighty years ago, in his novel The Jacob Street Mystery, R. Austin Freeman remarked:

To him that countryside, largely unspoiled in his early days, was an inexhaustible source of delight and a subject of endless study and meditation…And as the years passed and the countryside faded away under the withering touch of mechanical transport, that knowledge grew more and more precious. Now, the dwindling remnants had to be sought and found with considered judgement and their scanty material eked out with detail from the stores of the remembered past.

In his book The Romance of Natural History (1861), Philip Henry Gosse mentions a phenomenon known as blood rain:

At various times and in various places popular superstition has been excited by the occurrence of what have been called showers of blood. The destruction of cities and of kingdoms has been, according to historians, preceded by this awful omen. Yet this has been explained by a very natural and accountable phenomenon. In the year 1553, the hedges and trees, the stones of the pathway, and the clothes of many persons, were sprinkled copiously with drops of red fluid, which was supposed to be blood, till some observant person noticed the coincident appearance of unusual swarms of butterflies, and marked that the coloured drops proceeded from them.

The red drops were meconium, a waste substance produced by Lepidoptera shortly after they moult to adulthood. It indicates that there have been very large numbers of butterflies at certain times of the year. Many insects seem to be less abundant than they were forty years ago, almost certainly as a result of anthropogenic factors—intensive agriculture, urbanization, and, to a lesser extent, climate change and biological invasions. The last twenty years or so have seen scientific papers reporting declines in the numbers of ground beetles, dragonflies, moths, butterflies, and even caddisflies and some hemipterans. This is not a localized phenomenon but a global one, and not just from well-documented parts of Europe but also from more species-rich tropics, e.g. Costa Rica.

An increasing number of stories have appeared in the media in recent years, predicting insect apocalypse and ecological Armageddon. What does the research reveal? In 2017, Caspar Hallmann and colleagues reported a 75 per cent reduction in the biomass of flying insects in Germany over forty years, although the same sites were not sampled every year. And two years later, Sebastian Siebold and colleagues, again using data from Germany, showed similarly disturbingly high losses in biomass and abundance. Note that both of these studies were done in Germany, which is a heavily developed part of the planet.

There may be limitations in the data, but the take-home message that cannot be ignored is that many insect species, especially those associated with freshwater, are in steep decline. Even the most scathing of commentators do not dispute the fact that insects, in general, are in decline, and that the warnings should not be taken lightly. What all the research reporting insect declines and the burgeoning number of academic papers offering solutions have in common is that they reveal that the available data are very patchy in terms of insect orders covered and geographical locations.

There are reliable and robust long-term data sets showing the declines of butterflies and moths over the last half-century or so—although, again, the geographic coverage is largely confined to the UK, some parts of mainland Europe, and North America—and stories about this worrying trend attract a lot of media attention. Other charismatic groups, such as dragonflies and damselflies, are also in decline, as are the ubiquitous and equally charismatic ground beetles (carabids). But are other insects also in decline? Julie Ewald and colleagues from the Game and Wildlife Conservancy Trust, UK, analysed a remarkable forty-two-year data set on invertebrates in cereal fields in southern England and found that of the twenty-six invertebrate taxa studied less than half showed a decrease in abundance—spiders, braconid parasitic wasps, carabid beetles, Tachyporus beetles, Enicmus (scavenger beetles), cryptophagid fungus beetles, leaf-mining flies (agromyzids), fruit flies (Drosophila), Lonchopteridae (pointed-wing flies), and, surprisingly (or perhaps not), aphids. The other taxa showed no consistent pattern although bugs, excluding aphids, increased over the study period. More original recent work on British moths shows that, despite the overall picture of moths being in decline, some moth species, especially habitat generalists and some woodland specialists, have increased in abundance since 1968. Cereal fields are not, of course, a natural habitat and are intensely managed, with various pesticides being applied, so are perhaps not likely to be the most biodiverse or representative habitats to be found in the UK.

So what scientific evidence do we have for a decline in these less charismatic insects? Almost a hundred years ago, bibionid flies were regarded as a major pest, and forty years ago it was possible to catch almost 70,000 adults in traps in a four-week period from one field in southern England, suggesting that bibionids used to be very common. Only three of the Rothamsted Insect Survey traps showed downward trends in insect biomass over the thirty years (1973–2002) analysed, of which only the Hereford trap showed a significant decline. So, we are none the wiser. Two long-term studies that focus on a wider range of insect groups do not give a clear indication of insect decline, and both studies are limited in their geographic coverage so we do not know whether the results are representative of the whole country.

With the lack of funding for entomology, it is extremely difficult to get more robust data. Over a million insect species have been described to date and thousands more are described every year. Each species has a unique way of making a living: they eat different foods, live in different places, have different climatic requirements, reproduce at different rates, and have their own suite of natural enemies. Hardly any of them are monitored; those that are monitored are mainly pests. Globally only a few thousand people are collecting relevant data; considering that there are probably at least eight million insect species, the research barely scratches the surface, despite the magnificent efforts of the people involved in gathering this information. The Insectageddon stories are derived from a few local studies. Most are fine but there are not enough and they are too idiosyncratic for solid general conclusions. They are, however, believable, because in general they tell the same story—drastic declines over the last few decades—and they reflect what the older generation of entomologists have been reporting informally over the years.

Unlike some commentators who point their fingers directly at the use of pesticides as the major cause of decline, I am more inclined towards the idea of habitat degradation, fragmentation, and loss. It is long past time for governments around the world to invest much more into research in this area. We desperately need more properly replicated, well-designed, long-term studies to monitor the undeniable changes that are occurring.

Whether or not we believe that an ecological catastrophe is approaching, it is obvious that humans are having a marked effect on the biodiversity that keeps our planet in good working order, and not just through the need to feed an ever-increasing population. Recent studies have shown that our fixation with car ownership is killing billions of insects every year, and that our fear of the dark, and widespread use of artificial light, is putting insects and the animals that feed on them at risk.

For humans, with relatively short lifespans, shifting baselines can also be a problem. People accept what they have known in their childhoods as the natural state but it can work the other way: I remember in the early 1990s, when a particular butterfly species was at very low numbers compared with those that I and similar-aged colleagues remembered as children, the late British naturalist Miriam Rothschild telling me how as a girl, in the 1920s, she had conversely remembered their numbers as being very low. Her message was to consider also the ‘populations cycle’. It is because of this propensity, which is nicely illustrated by some of my own twenty-year data sets, all from the same fifty-two sycamore trees at Silwood Park, Berkshire, UK, that we need access to long-term funding to monitor insect populations. Chop my data sets into three-year periods, the length of a typical PhD study or research grant, and you see some very different pictures of the populations of three common insect species (Figure 31).

31. Changes in abundance of three common insect species over a twenty-year period: winter moth, Operophtera brumata (top); the sycamore aphid, Drepanosiphum platanoidis (middle); the maple aphid, Periphyllus testudinaceus (bottom). The populations can be seen to fluctuate over twenty years.

Given these fluctuations in populations, the fact that most of the evidence for insect declines is based largely on studies from Europe, primarily the UK, and that the evidence from tropical locations has been subject to alternative interpretations, there is an urgent need for action.

First, we need to build on the work that has been done in Germany by scientists like Caspar Hallmann, and in the UK via the Rothamsted Insect Survey and the Biological Records Centre (UK Centre for Ecology & Hydrology), and establish active insect monitoring networks using repeatable sampling methods but on a global scale. New monitoring programmes will not help to establish past baselines but they can help us to determine trends from this point forward. We can make this truly global by engaging the public through community (citizen) science. Programmes will need to use standardized, commonly and easily used methods, such as Malaise traps, pitfall traps, light traps, and effort-based counts, with species diversity, abundance, and biomass being primary measures. Although biomass is an imperfect estimator because it can be sensitive to changes in abundance of large species, it is a valuable metric from the ecosystem perspective. Determining biomass trends does not require fine-scale taxonomic knowledge, which is often lacking in community science initiatives. Even if it were possible, it would be incredibly expensive to try to monitor all insect species from any community with appreciable diversity. A much better option, and one that will certainly appeal to a wide range of community scientists, would be to monitor taxa like butterflies, macro-moths, dragonflies, bees, and some beetle groups. All these can serve as indicator species for other insect groups and, tongue in cheek, many can be observed using binoculars, thus encouraging ornithologists and mammalogists to join in.

There are already a few long-term national monitoring schemes. For example, the Environmental Change Network collects biotic and abiotic data, including many insect groups, from fifty-seven sites across the UK using identical protocols. Multiple Long-Term Ecological Research (LTER) projects track different facets of ecosystems in different ways. In fact, if expanded to a global scale, the LTER network could be the natural framework to make a global network proposal feasible, possibly through targeted funding. Unfortunately, all the active long-term monitoring schemes are younger than modern agricultural intensification. We need to use museum collections and pre-1940s entomological journals to construct data sets. Some long-term historical datasets are already accessible, such as the 150-year record of pine beauty moth infestations in Germany dating from 1810.

Whatever we do, it will need long-term funding that is stable, substantial, and sustained. Entomological survey and monitoring work may appear mundane but is essential given the importance of insects to the health of ecosystems. Funding should reflect the diversity and abundance of taxa, not their perceived charisma. The focus of major donors needs to shift from insect eradication to insect conservation.

We also need to act quickly; there is no Planet B. I am, however, not hopeful. Despite the many ‘Insectageddon’ stories, the majority of young researchers tend to focus on vertebrates, many in exotic locations, continuing a pattern noted many years ago.

An underappreciation of the importance of insects is widespread, so much so that it might be time to coin some new words to describe it: entomyopia, entomological short-sightedness, and entoalexia, insect blindness. A better general understanding of the natural world and the role of insects is essential if we are to prevent any further inroads into their existence. As this book has shown, insects are not just pests and pollinators; they are part of the very fabric of our existence.

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Chapter 6: Mimicry, crypsis, and blatant advertising

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Chapter 7: Against the odds

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Chapter 8: The good, the bad, and the ugly

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Root, R. B. (1973) Organization of a plant-arthropod association in simple and diverse habitats: The fauna of collards. Ecological Monographs, 43, 95–124.

Tahvanainen, J., and Root, R. B. (1972) The influence of vegetational diversity on the population ecology of a specialized herbivore Phyllotreta cruciferae (Coleoptera: Chrysomelidae). Oecologia, 10, 321–46.

Ullyett, G. C. (1947) Mortality factors in populations of Plutella maculipennis Curtis (Tineidae: Lep.) and their relation to the problem of control. Union of South Africa, Department of Agriculture and Forestry Entomology Memoirs, 2, 77–202.

Chapter 9: Ecological Armageddon—insects in decline?

Dirzo, R., Young, H. S., Galetti, M., Ceballos, G., Isaac, N. J. B., and Collen, B. (2014) Defaunation in the Anthropocene. Science, 345, 401–6.

Ewald, J., Wheatley, C. J., Aebsicher, N. J., Moreby, S. J., Duffield, S. J., Crick, H. Q. P., and Morecroft, M. B. (2015) Influences of extreme weather, climate and pesticide use on invertebrates in cereal fields over 42 years. Global Change Biology, 21, 3931–50.

Fox, R. (2013) The decline of moths in Great Britain: A review of possible causes. Insect Conservation & Diversity, 6, 5–19.

Hallmann, C. A., Sorg, M., Jongejans, E., Siepel, H., Hoflan, N., Schwan, H., Stenmans, W., Muller, A., Sumser, H., Horren, T., Goulson, D., and De Kroon, H. (2017) More than 75 percent decline over 27 years in total flying insect biomass in protected areas. PLoSONE, 12(10), e0185809.

Møller, A. P. (2019) Parallel declines in abundance of insects and insectivorous birds in Denmark over 22 years. Ecology & Evolution, 9, 6581–7.

Montgomery, G. A., Dunn, R. R., Fox, R., Jongejans, E., Leather, S. R., Saunders, M., Shortall, C. R., Tingley, M. W., and Wagner, D. L. (2020) Is the insect apocalypse upon us? How to find out. Biological Conservation.

Reemer, M., van Helsdingen, P. J., and Kleukers, R. M. J. C. (2003) Changes in ranges: Invertebrates on the move. Proceedings of the 13th International Colloquium of the European Invertebrate Survey, Leiden, 2–5 September 2001, European Invertebrate Survey, The Netherlands.

Sánchez-Bayo, F., and Wyckhuys, K. A. G. (2019) Worldwide decline of the entomofauna: A review of its drivers. Biological Conservation, 232, 8–27.

Shortall, C. R., Moore, A., Smith, E., Hall, M. J., Woiwod, I. P., and Harrington, R. (2009) Long-term changes in the abundance of flying insects. Insect Conservation & Diversity, 2, 251–60.

Wepprich, T., Adrion, J. R., Ries, L., Wiedmann, J., and Haddad, N. M. (2019) Butterfly abundance declines over 20 years of systematic monitoring in Ohio, USA. PLoS ONE, 14(7), e0216270.

Further reading

General

Chapman, R. F., Simpson, S., and Douglas, A. E. (2013) The Insects: Structure and Function, Fifth Edition, Cambridge University Press, Cambridge.

Gillott, C. (2005) Entomology, Springer, Dordrecht.

Gullan, P. J., and Cranston, P. S. (2014) The Insects: An Outline of Entomology, Fifth Edition, Wiley-Blackwell, Oxford.

Chapter 1: In the beginning

Footit, R. G., and Adler, P. H. (2017) Insect Biodiversity: Science and Society, Volume 1, Wiley-Blackwell, Oxford.

Grimaldi. D., and Engel, M. S. (2005) Evolution of Insects, Cambridge University Press, New York.

McAlister, A. (2017) The Secret Life of Flies, Natural History Museum, London.

Chapter 2: Prolific procreators

Leather, S. R. (1995) Insect Reproduction, CRC Press, Boca Raton, FL.

Chapter 3: On the move

Alexander, D. E. (2015) On the Wing, Oxford University Press, Oxford.

Bernays, E. A., and Chapman, R. F. (1994) Host Plant Selection by Phytophagous Insects, Chapman & Hall, New York.

Chapter 4: Living together

Wilson, E. O. (1975) Sociobiology: The New Synthesis, Harvard University Press, Cambridge, MA.

Chapter 5: Aquatic insects

Corbet, P. S., and Brooks, S. J. (2008) Dragonflies, Collins, London.

Del Claro, K., and Guillermo, R. (2019) Aquatic Insects: Behavior and Ecology, Springer, Dordrecht.

Chapter 6: Mimicry, crypsis, and blatant advertising

Clifton, J., and Wheeler, J. R. (2011) Bird-dropping Tortrix Moths of the British Isles: A Field Guide to the Bird-dropping Mimics.

Quicke, D. L. J (2016) Mimicry, Crypsis, Masquerade and other Adaptive Resemblances, Wiley-Blackwell, Oxford.

Chapter 7: Against the odds

Alcock, J. (1997) In a Desert Garden: Love and Death Among the Insects, W.W. Norton & Co, New York.

Leather, S. R., Bale, J. S., and Walters, K. F. A. (1993) The Ecology of Insect Overwintering, Cambridge University Press, Cambridge.

Chapter 8: The good, the bad, and the ugly

Abrol, D. P. (Ed.), (2013) Integrated Pest Management: Current Concepts and Ecological Perspective, Elsevier, Amsterdam.

Godfray, H. C. J. (1995) Parasitoids: Behavioral and Evolutionary Ecology, Princeton University Press, Princeton, NJ.

Heimpel, G. E., and Mills, N. J. (2017) Biological Control: Ecology and Applications, Cambridge University Press, Cambridge.

McAlister, E. (2016) The Secret Life of Flies, Natural History Museum, London.

Ulyshen, M. D. (Ed.) (2018) Saproxylic Insects: Diversity, Ecology and Conservation, Springer, Dordrecht.

Chapter 9: Ecological Armageddon—insects in decline?

New, T. R. (2016) Alien Species and Insect Conservation, Springer-Verlag, Dordrecht.

Samways, M. J. (2020) Insect Conservation: A Global Synthesis, CABI, Wallingford.

Index

For the benefit of digital users, indexed terms that span two pages (e.g., 52–53) may, on occasion, appear on only one of those pages.

A

abdomen  5–6

advertising  89–91

aggregations  47

alderfly  17

Alexander, David  36

alfalfa aphid (Acyrthosiphon kondoi)  97

Allee, W. C.  xxiii

ambrosia beetle  120–121

ametabolous lifecycle  11–13

angel insect  14

antennae  9–10

origins  2–3

anthophilous insects  113–114

antlers  32

ants  17, 37–38

association with aphids  53–58

association with plants  58–59

social behaviour  48, 50

aphids  13–19

aggregations  47

association with ants  53–58

colour  58, 61–62

defence mechanisms  54

migration  39–41

reproductive system  23–25

response to drought  100–101

spreaders of diseases  107

subsociality  52–53

symbiotic relationships  60

apterous insects (wingless)  13–18

Apterygota  13

aquatic insects  66

Ephemeroptera  70–71

marine environments  78–80

types  68–69

see also hydrophiles

arborophiles  38–39

see also trees

Archaeognatha  13

armyworm (Spodoptera eridania)  39–40, 44–45

arthropods  1–2

assassin bug (Stenolemus bituberus)  84–85

associational resistance  104–105

B

bacteria, symbiotic relationships  60–61

bark beetle  120–121

bark louse  14

Bates, Henry  82–83

bed bug

reproductive system  23–25

symbiotic relationships  59–60

bee orchid (Ophrys apifera)  115–117

bees  17

communication  49

pollination  115–117

social behaviour  47–48

beet aphid (Pemphigus betae)  52–53

beetles  17, 21–22

desert environments  97

flightless  38–39

saproxylic  117–119

bibionid flies  125–126

biological control  109–113

black bean aphid (Aphis fabae)  56, 58

black cherry  58–59

black garden ant (Lasius niger)  56

black spruce aphid (Cinara picaea)  39–40

black willow bark aphid (Pterocomma salicis)  56

blood rain  123–124

blowflies  121–122

body structure  xxi, 5–6

honeybee (Apis mellifera)  6

book louse  14

bounded ignorance  37–39

brain  9

breeding  23

bristletail  13

buff tip (Phalera bucephala)  83–84

bumblebees  114–115

burrower bug (Sehirus cinctus)  52

burying beetles  121–122

butterflies  17

aggregations  47

attraction to colours  115

in decline  125

lifecycle  11–12, 19

migration  39–40

mimicry  81–85

sexual selection  32

C

cabbage root fly (Delia radicum)  94–96

cabbages  44–45

cabbage white butterfly (Pieris rapae)

diet  44–45

egg-laying  28–29

caddisfly  17, 67, 75–78

camouflage  83–87

capital breeders  25–26

carabid beetles  38–39, 98–99, 125

carrion beetle  51

carrion feeders  121–122

Chathamiidae  77

Chemical Interference Hypothesis  105–106

Cheng, Dr Lanna  78–79

chinch bug  14

cinnabar moth  89–90

circulatory system  8–9

classification of insects  3, 5

Cleveland, Lemuel Roscoe  48

click beetle (Agriotes lineatus)  98

climate  92–101

cockroach  14

coevolutionary arms race  44–45

Coleoptera  17, 19, 21–22

wings  35–36

collectors  68

colour

advertising toxicity  89–91

aphids  58, 61–62

as a defence mechanism  86–87

distractive/disruptive marking  88–89

of flowers  115

comma butterfly (Polygonia c-album)  85

communication  49

conehead  13

coprophagy  121–122

corpora allata  10–11

corpora cardiaca  10–11

cottony cushion scale (Icerya purchasi)  110

crane fly  98

cricket  14, 33–34

crustaceans  3, 5, 78–79

cuticle  6

cytokinin  63–65

D

Dajoz, Roger  117–118

damselfly  2–3, 14, 69, 73–75

in decline  125

dance fly (Empis borealis)  31

darkling beetle (Stenocara gracilipes)  92

Darlington, Philip  38–39

Darwin, Charles  38–39, 114–115

Darwin, Erasmus  109–110

day length  94

DeBach, Paul  111

defence mechanisms  xxii

of aphids  54

camouflage  83–87

colouration  86–87

mimicry  81–85

of plants  45, 108–109

toxins  81

Denno, Bob  99–100

Dermaptera  14

desert environments  96–97

detoxification  44–45

diamondback moth (Plutella xylostella)  44–45, 103–104

Dictyoptera  14

diet  xxi–xxii, 19–21, 41–46

catching food  77

Diplura  13

Diptera  17, 19

directed aerial descent  37–38

discontinuous ventilation  96–97

diseases, insects as vectors  107

distractive/disruptive marking  88–89

diversity  xxi–xxiii

diving beetle  66–67

Dixon, Tony  40–41

dobsonfly  17

domestication  xxi–xxii

dragonfly  2–3, 14, 35, 73–75

in decline  125

larvae  74

legends  75

drought  97–101

Dudley, Robert  37–38

dung beetle  51, 122

dung feeders  121–122

E

earwig  14, 52

ecdysteroids  10–11

ecosystems  xxii

Edgerly-Rooks, Janice  14

eggar moth  27–28

egg parasitoid wasp (Pseudoligosita longifrangiata)  69

eggs  26–29

camouflage  86–87

clusters  27–28

hydration  98

Odonata  73–74

parental care  51–52

Elton, Charles  39–40, 103–104

Embioptera  14

endangered insects  71–72

Endopterygota  13, 17

wings  17

enemies hypothesis  103–104

Engelbrecht, Lisabeth  63

Entognatha  1–3

Ephemeroptera  14, 35–36

aquatic  70–71

swarms  31

ermine moth  27–28

Erwin, Terry  12

Eucalyptus lerp (Cardiaspina densitexta)  99

evolution  2–4

of flight  36–39

Ewald, Julie  125

Exopterygota  13–14

wings  13–18

exoskeleton  xxi–xxii

chitinous  1–3

difficulties with respiratory system  8

moulting  1

structure  6

eyed hawkmoth (Smerinthus ocellata)  85

eyes  9–10

on stalks  31

F

fecundity  25–26

and migration  40–41

feet, sensory organs  9–10

fighting

aphids  52–53

stag beetle  32

Fischer, Christophe  58

flea  12–13, 17

flesh flies  121–122

flight  35

evolutionary theories  36–39

migration  39–41 see also wings

flowers

colour  115

scent  115

flush feeders  43–45

fly  17

fly orchid (Ophrys insectiflora)  116

fossils  3–5, 36

Freeman, R. Austin  123

freezing temperatures  92–96

funding for research  xxiii

fungi  118, 120–121

G

galls  52–53

ganglia  9

geophiles  38–39

gerrids  79–80

ghost midge (Chaoborus flavica)  31

giant oak aphid (Stomaphis quercus)  56

gills  67

gill theory  36–37

Giron, David  63

gladiator (Mantophasmatodea)  14

Goedaert, Jan  53

Gosse, Philip Henry  123–124

grain aphid (Sitobion avenae)  92–94

grasshopper  11–12, 14

great purple hairstreak butterfly (Atlides halesus)  32

green islands  62–65

ground beetles (carabids)  38–39, 98–99, 125

growth and development  10–11

H

habitats  xxi, 5, 19–21

of flightless beetles  38–39

haemolymph  8–9, 96–97

Haldane, J. B. S.  21–22

Hallmann, Caspar  124, 129

Halobates  79–80

halteres  17

hanging fly  17

Harlequin ladybird (Harmonia axyridis)  111–113

heads  5–6

Heard, Stephen  17

heat, extremes of  96–97

hemimetabolous lifecycle  11–13

Hemiptera  14, 19–21

aggregations  47

herbaceous plants  41–42

Heteroptera  14

hexapods  1–3

hill topping  32

Hinde, Rosalind  60–61

Holometabola  35–36

holometabolous lifecycle  11–13, 19

overwintering  94–95

Homoptera  14

honeybee (Apis mellifera)  xxi–xxii, 47–48, 114

body structure  6

hormones  10–11

housefly  7

sensory organs  9–10

hoverfly  25

as predators  108

Huberty, Susan  99–100

hummingbird hawkmoth (Macroglossum stellatarum)  29

Huxley, Thomas Henry  60

hydration  97–101

hydrophiles  38–39, see also aquatic insects

Hydroptilidae  69

Hymenoptera  17, 21–22

I

ice crawler (Grylloblattodea)  14, 19–21

Idiobionts  112

income breeders  25–26

Indian stick insect  86

insects

in decline  123

diversity  xxi–xxiii

evolution  2–4

importance of  102–103, 113–122

numbers of species  12, 21–22

origins  1–5

intercropping  105–106

J

Janzen, Dan  58–59

jumping bristletails  2–3

juvenile hormones  10–11

K

Kaiser, Wilfried  64–65

Kingsolver, Joel  37–38

kissing bug (Rhodnius prolixus)  10–11

Koebele, Albert  110–111

Koehl, Mimi  37–38

Koenig, Alexander  3

Koinobionts  112

L

lacewing  7, 17

ladybird beetle  25

ladybirds

aggregations  47

egg-laying  27–28

as predators  108

response to drought  100–101

lappet moth (Gastropacha quercifolia)  27–28, 88–89

large blue butterfly (Phenagris arion)  84–85

larvae  2–3, 11–12

aquatic  67, 69, 76

body structure  5–6

diet  25, 45–46

hydration  98

Odonata  74–75

leaf insect  14

leaf-mining  63–65

leaves, toughness  41–43

legs  5–6

leks  31

Lepidoptera  17

diet  41–42, 44–46

hill topping  32

lifecycle  11–12

oviposition  27–29

similarity to Trichoptera  76

spermatophores  33–34

lichen katydid (Markia hystrix)  86

lifecycle  2–3, 10–12

locomotion  35–46

flight see flight

locust  39–40

Long-Term Ecological Research (LTER)  129–130

louse  14

Lyell, Charles  38

M

Madeira, island of  38–39

mandibles, modified  32

mantid  14, 32–33

Mantodea  14

map butterfly (Araschnia evana)  87

maple aphid (Periphyllus testudinaceus)  55, 57, 128

marine insects  66, 78–80

marsh helleborine orchid (Epipactis veratrifolia)  116

maternal provisioning  51

mating  29–30

behaviours  31–32

death during  32–33

nuptial gifts  29–30, 32–34

sex pheromones  30

mayfly  2–3, 14, 70–71

gill theory  36–37

swarms  31, 70–71

meconium  124

Mecoptera  17

medicinal properties  xxi–xxii

Megaloptera  17

Merveille du Jour (Griposia aprilina)  86

metamorphosis  10–11

complete  11–12, 19

incomplete  11–12

midge, swarms  31

migration  39–41

mimicry  81–85

mining bee (Eucera longicornis)  115–117

Mishof, Bernhard  3

monarch butterfly (Danaus plexippus)  29, 33–34

aggregations  47

colour  89–90

migration  39–40

monkshood aphid (Delphiniobium junackianum)  91

Moran, Nancy  61

Morgan’s sphinx moth (Xanthopan morgani praedicta)  114–115

mosquito  25–26, 67

spreaders of diseases  107

moths  17

in decline  125

lifecycle  11–12, 19

oviposition  27–28

response to sex pheromones  30

moulting  1, 10–11

mountain birch (Betula pubescens)  58–59

mouthparts  3

in pollination  114–115

position  14

Muffet, Thomas  75–76

mugwort aphid (Macrosiphoniella yomogicola)  58

Müller, Johann  82–83

mutualism  53–62

N

necrophagy  121–122

nervous system  xxii, 9–10

neurohormones  10–11

Neuroptera  17

Nordaustlandet island  39–40

Notoptera  14

numbers of insects, in decline  123

numbers of insect species  12, 21–22

nun moth (Lymantria monacha)  58–59

nuptial gifts  29–30, 32–34

nutritional efficiency complex  41–42

O

oak tree hopper (Platycotis vittata)  52

ocelli (eyes)  9–10

Odonata  14, 19–21, 35–36, 73–75

offspring  25–26

oligophages  43–44

orchids  115–117

orders  12–22

Orthoptera  14, 19–21, 35–36

nuptial gifts  33

ovarioles  23

in aphids  40–41

overwintering  94–96

oviposition  17, 25–29

in wood  119

P

painted lady butterfly  39–40

paranotal lobe theory  37

parasites  21–22, 25, 69, 104–105, 107–113

parasitic wasp  xxi, 94

parasitoids  108–109, 112

parenting  25–27, 49–52

joint responsibility  51–52

parthenogenetic insects  23–25

pea aphid (Acyrthosiphon pisum)  61–62

peach-potato aphid (Myzus persicae)  43–44

peacock butterfly (Inachis io)  85

Peklo, Jaroslav  60

peppered moth (Biston betularia)  86

pests  103–107

biological control  109–113

Phasmotodea  14

pheromones  30

to attract pollinators  116

for communication  49

detection  9–10

Phthiraptera  14

phylogenetic trees  3, 5, 20

orders  12–22

piercers  69

pine beauty moth (Panolis flammea)  26–27, 95–96, 108–109

pitcher plant mosquito (Wyeoymia smithii)  66

plants

association with ants  58–59

colour  115

defence mechanisms  45, 108–109

green islands  62–65

scent  115

toughness  41–43

plant-stress hypothesis  99–100

Plecoptera  14, 71–73

plum weevil  110

pollen feeders  115–116

pollination  102, 113–116

Polyneoptera  20, 35–36

polyphages  43–44

pond skater  67

Pontin, John  54

populations cycle  127

praying mantis  14, 32–33

predators  69, 73–74, 104–105, 107–113

processionary moth  27–28

prothoracic glands  10–11

Protura  13

Psocoptera  14

pulsatile dorsal vessel  8–9

pupae  11–12

purple edged copper butterfly (Lycaena hippothoe)  32

R

rape pollen beetle (Brassicogethes aeneus)  113–114

rat-tailed syrphid  67

Remipedia  2–3

reproductive system  23–25

resource concentration hypothesis  104–105

respiratory system  5, 8, 67

discontinuous ventilation  96–97

Rhapidioptera  17

Rhoades, Doug  99

rice stem borer (Chilo partellus)  28–29

Riley, Charles  110–111

Root, Richard  104–105

rose aphid (Macrospihum rosae)  61

Rothschild, Miriam  127

S

sabre wasp (Rhyssa persuasoria)  119

saproxylics  116–121

scent  115

scorpionfly  17, 32–33

scrapers  68

Scriber, Mark  41–42

sea skater  xxi

seasonal variations  92–101

secondary sexual characteristics  30

senescence  62–63

senescence feeders  43–44

sensory organs  9–10, 115

sexton beetle  51, 121–122

sexual selection  29–30

behaviours  31–32

death during copulation  32–33

nuptial gifts  29–30, 32–34

pheromones  30

Shaw, Michael  40–41

shredders  68

Siebold, Sebastian  124

silk moth  xxi–xxii

silphids  51, 121–122

silverfish  2–3, 13

Siphonaptera  17

sizes of insects  xxi, 8

Skinner, Gary  57

Skoog, Folke  62

Slansky, Frank  41–42

small tortoiseshell butterfly (Aglais urticae)  85

snakefly  17

social behaviour  xxi–xxii, 2–3, 47–65

in extreme temperatures  94

soldier aphids  53

southern mole cricket (Scapteriscus borelli)  98

speckled wood butterfly (Pararge aegeria)  32–34

sperm  23–25

spermatophores  29–30, 33–34

spiracular systems  67–68, 96–97

stag beetle  32

Staley, Joanna  100–101

stalk-eyed fly  30–31

stick insect  14

reproductive system  23–25

stonefly  14, 71–73

Stork, Nigel  21–22

Strepsiptera  17

subimago  70–71

subsociality  51–53

succession  118–120

supercooling  92–94

super-orders  13–18

survival  xxii

swallowtail butterfly (Papilio machaon/polyxenes)  32, 44–45

swarms  31

swollen thorn acacia  58–59

sycamore aphid (Drepanosiphum platanoidis)  55, 57, 128

symbiosis  xxii

symbiotic relationships  53–62

T

Tahvanainen, Jarmo  104–106

Taylor, Roy  39–40

temperature  92–101

termites  14

communication  49

social behaviour  48–50

symbiotic relationships  59–60

thorax  5–6

thrips  14, 19–21

thunderfly/thunderbug (thrips)  14, 19–21

Thysanoptera  14, 19–21

Tielka, Eirik  12–13

Tilman, Dave  58–59

titan beetle (Titanus giganteus)  xxi

Tóth, László  60

toxicity  81, 89–91

traumatic insemination  23–25

trees  41–42, see also arborophiles

trichogrammid wasp (Trichogramma julianoi)  69

Trichoptera  17, 68, 75–78

trophobiosis  55

tropical aphid (Aphis gossypii)  97

true bugs  52

Trumbo, Stephen  51

Tsuchida, Tsutomo  61–62

tussock moth  27–28

U

Ullyett, George  103–104

uses of insects  xxi–xxii

V

van Bruyssel, Ernest  53

vapourer moth (Orgyia antiqua)  51

vetch aphid (Megoura vicia)  94

vine weevil (Otiorhynchus sulcatus)  8

reproductive system  23–25

viruses  107

von Eschscholtz, Johann Friedrich Gustav  79–80

W

Walters, Keith  40–41

Walton, Izaak  75–76

wasps  17

egg parasitoid wasp (Pseudoligosita longifrangiata)  69

parasitic wasp  xxi, 94

sabre wasp (Rhyssa persuasoria)  119

saproxylic  119

trichogrammid wasp (Trichogramma julianoi)  69

wood wasp (Sirex noctilo)  119

Watanabe, Saori  58

water boatman  67

web spinner  14

weevil (Sitona hispidulus)  98

weevil (Strophosomus toimmelanocephalus)  94–95

Western corn rootworm (Diabrotica virgifera)  98

White, Tom  99

Whittaker, John  57

Wigglesworth, Sir Vincent  10–11

Wiklund, Christer  85

willow aphid (Tuberolacnhus salignus)  56

Wilson, David  51

wings  35

absence (aperous insects)  13–18

bounded ignorance approach  37–39

Endopterygota  17

Exopterygota  13–18

functionality  8

gill theory  36–37

Greek and Latin words  13

Odonata  73

origins  2–3

paranotal lobe theory  37

position  5–6

structure  7–8

thrips  21

winter moth (Operophtera brumata)  43–46, 128

Wollaston, Vernon  38

wood  116–121

wood ant (Formica rufa)  57

wood tiger moth (Arctia plantaginis)  90

wood wasp (Sirex noctilo)  119

Y

Yanoviak, Steve  37–38

yellow meadow ant (Lasius flavus)  54

Z

Zoraptera  14, 19–21

Zygentoma  13

The History of Life

A Very Short Introduction

Michael J. Benton

There are few stories more remarkable than the evolution of life on earth. This Very Short Introduction presents a succinct guide to the key episodes in that story - from the very origins of life four million years ago to the extraordinary diversity of species around the globe today. Beginning with an explanation of the controversies surrounding the birth of life itself, each following chapter tells of a major breakthrough that made new forms of life possible: including sex and multicellularity, hard skeletons, and the move to land. Along the way, we witness the greatest mass extinction, the first forests, the rise of modern ecosystems, and, most recently, conscious humans.

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Game Theory

A Very Short Introduction

Ken Binmore

Games are played everywhere: from economics to evolutionary biology, and from social interactions to online auctions. Game theory is about how to play such games in a rational way, and how to maximize their outcomes. Game theory has seen spectacular successes in evolutionary biology and economics, and is beginning to revolutionize other disciplines from psychology to political science. This Very Short Introduction shows how game theory can be understood without mathematical equations, and reveals that everything from how to play poker optimally to the sex ratio among bees can be understood by anyone willing to think seriously about the problem.

www.oup.com/vsi