animal life encyclopedia

Grzimek’s Animal Life Encyclopedia, Second Edition Volume 2: Protostomes Produced by Schlager Group Inc.. I amtherefore extremely proud to have served as the series editor for the Gale G

Grzimek’s Animal Life Encyclopedia

Second Edition

● ● ● ●

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Grzimek’s Animal Life Encyclopedia

Second Edition

● ● ● ● Volume 2 Protostomes

Sean F Craig, Advisory Editor Dennis A Thoney, Advisory Editor

Neil Schlager, Editor Joseph E Trumpey, Chief Scientific Illustrator

Michael Hutchins, Series Editor

I n a s s o c i a t i o n w i t h t h e A m e r i c a n Z o o a n d A q u a r i u m A s s o c i a t i o n

Project Editor

Melissa C McDade

Editorial

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Kretschmann, Mark Springer

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Recommended citation: Grzimek’s Animal Life Encyclopedia, 2nd edition Volume 2, Protostomes, edited by Michael Hutchins, Sean F Craig, Dennis A Thoney,

and Neil Schlager Farmington Hills, MI: Gale Group, 2003.

Grzimek’s Animal Life Encyclopedia, Second Edition

Volume 2: Protostomes Produced by Schlager Group Inc.

Neil Schlager, Editor Vanessa Torrado-Caputo, Associate Editor

LIBRARY OF CONGRESS CATALOGING-IN-PUBLICATION DATA

Grzimek, Bernhard.

[Tierleben English]

Grzimek’s animal life encyclopedia.— 2nd ed.

v cm.

Includes bibliographical references.

Contents: v 1 Lower metazoans and lesser deuterosomes / Neil Schlager, editor — v 2 Protostomes / Neil Schlager, editor — v 3 Insects / Neil Schlager, editor — v 4-5 Fishes I-II / Neil Schlager, editor —v 6 Amphibians / Neil Schlager, editor — v 7 Reptiles / Neil Schlager, editor — v 8-11 Birds I-IV / Donna Olendorf, editor — v 12-16 Mammals I-V / Melissa C McDade, editor — v.

17 Cumulative index / Melissa C McDade, editor.

ISBN 0-7876-5362-4 (set hardcover : alk paper)

1 Zoology—Encyclopedias I Title: Animal life encyclopedia II.

Schlager, Neil, 1966- III Olendorf, Donna IV McDade, Melissa C V American Zoo and Aquarium Association VI Title.

QL7 G7813 2004

590’.3—dc21 2002003351

Disclaimer:

Some images contained in the original version of this book are not available for inclusion

in the eBook

Foreword viii

How to use this book x

Advisory board xiii

Contributing writers xv

Contributing illustrators xvii

Volume 2: Protostomes What is a protostome? 3

Evolution and systematics 7

Reproduction, development, and life history 15

Ecology 25

Symbiosis 31

Behavior 35

Protostomes and humans 41

Phylum ANNELIDA Class POLYCHAETA 45

Class MYZOSTOMIDA 59

Class OLIGOCHAETA 65

Class HIRUDINIDA 75

Class POGONOPHORA 85

Phylum VESTIMENTIFERA 91

Phylum SIPUNCULA 97

Phylum ECHIURA 103

Phylum ONYCHOPHORA 109

Phylum TARDIGRADA 115

Phylum ARTHROPODA Subphylum CRUSTACEA Class REMIPEDIA 125

Class CEPHALOCARIDA 131

Class BRANCHIOPODA Order ANOSTRACA 135

Order NOTOSTRACA 141

Order CONCHOSTRACA 147

Order CLADOCERA 153

Class MALACOSTRACA Subclass PHYLLOCARIDA 161

Subclass EUMALACOSTRACA Order STOMATOPODA 167

Order BATHYNELLACEA 177

Order ANASPIDACEA 181

Order EUPHAUSIACEA 185

Order AMPHIONIDACEA 195

Order DECAPODA 197

Order MYSIDA 215

Order LOPHOGASTRIDA 225

Order CUMACEA 229

Order TANAIDACEA 235

Order MICTACEA 241

Order SPELAEOGRIPHACEA 243

Order THERMOSBAENACEA 245

Order ISOPODA 249

Order AMPHIPODA 261

Class MAXILLOPODA Subclass THECOSTRACA 273

Subclass TANTULOCARIDA 283

Subclass BRANCHIURA 289

Subclass MYSTACOCARIDA 295

Subclass COPEPODA 299

Subclass OSTRACODA 311

Class PENTASTOMIDA 317

Subphylum CHELICERIFORMES Class PYCNOGONIDA 321

Class CHELICERATA Subclass MEROSTOMATA 327

Subclass ARACHNIDA 333

Subphylum UNIRAMIA Class MYRIAPODA Subclass CHILOPODA 353

Subclass DIPLOPODA 363

Subclass SYMPHYLA 371

Subclass PAUROPODA 375

Phylum MOLLUSCA Class APLACOPHORA 379

• • • • •

Contents

Class MONOPLACOPHORA 387

Class POLYPLACOPHORA 393

Class GASTROPODA Subclass OPISTHOBRANCHIA 403

Subclass PULMONATA 411

Order PATELLOGASTROPODA 423

Superorder VETIGASTROPODA 429

Order COCCULINIFORMIA 435

Order NERITOPSINA 439

Order CAENOGASTROPODA 445

Class BIVALVIA 451

Class SCAPHOPODA 469

Class CEPHALOPODA 475

Phylum PHORONIDA 491

Phylum ECTOPROCTA Class PHYLACTOLAEMATA 497

Class STENOLAEMATA 503

Class GYMNOLAEMATA 509

Phylum BRACHIOPODA Class INARTICULATA 515

Class ARTICULATA 521

For further reading 529

Organizations 534

Contributors to the first edition 535

Glossary 542

Protostomes order list 548

Geologic time scale 550

Index 551

Earth is teeming with life No one knows exactly how many

distinct organisms inhabit our planet, but more than 5

mil-lion different species of animals and plants could exist,

rang-ing from microscopic algae and bacteria to gigantic elephants,

redwood trees and blue whales Yet, throughout this

won-derful tapestry of living creatures, there runs a single thread:

Deoxyribonucleic acid or DNA The existence of DNA, an

elegant, twisted organic molecule that is the building block

of all life, is perhaps the best evidence that all living

organ-isms on this planet share a common ancestry Our ancient

connection to the living world may drive our curiosity, and

perhaps also explain our seemingly insatiable desire for

in-formation about animals and nature Noted zoologist, E O

Wilson, recently coined the term “biophilia” to describe this

phenomenon The term is derived from the Greek bios

mean-ing “life” and philos meanmean-ing “love.” Wilson argues that we

are human because of our innate affinity to and interest in the

other organisms with which we share our planet They are,

as he says, “the matrix in which the human mind originated

and is permanently rooted.” To put it simply and

metaphor-ically, our love for nature flows in our blood and is deeply

en-grained in both our psyche and cultural traditions

Our own personal awakenings to the natural world are as

diverse as humanity itself I spent my early childhood in rural

Iowa where nature was an integral part of my life My father

and I spent many hours collecting, identifying and studying

local insects, amphibians and reptiles These experiences had

a significant impact on my early intellectual and even

spiri-tual development One event I can recall most vividly I had

collected a cocoon in a field near my home in early spring

The large, silky capsule was attached to a stick I brought the

cocoon back to my room and placed it in a jar on top of my

dresser I remember waking one morning and, there, perched

on the tip of the stick was a large moth, slowly moving its

delicate, light green wings in the early morning sunlight It

took my breath away To my inexperienced eyes, it was one

of the most beautiful things I had ever seen I knew it was a

moth, but did not know which species Upon closer

exami-nation, I noticed two moon-like markings on the wings and

also noted that the wings had long “tails”, much like the

ubiq-uitous tiger swallow-tail butterflies that visited the lilac bush

in our backyard Not wanting to suffer my ignorance any

longer, I reached immediately for my Golden Guide to North

American Insects and searched through the section on moths

and butterflies It was a luna moth! My heart was poundingwith the excitement of new knowledge as I ran to share thediscovery with my parents

I consider myself very fortunate to have made a living as

a professional biologist and conservationist for the past 20years I’ve traveled to over 30 countries and six continents tostudy and photograph wildlife or to attend related conferencesand meetings Yet, each time I encounter a new and unusualanimal or habitat my heart still races with the same excite-ment of my youth If this is biophilia, then I certainly possess

it, and it is my hope that others will experience it too I amtherefore extremely proud to have served as the series editor

for the Gale Group’s rewrite of Grzimek’s Animal Life

Ency-clopedia, one of the best known and widely used reference

works on the animal world Grzimek’s is a celebration of

an-imals, a snapshot of our current knowledge of the Earth’s credible range of biological diversity Although many other

in-animal encyclopedias exist, Grzimek’s Animal Life Encyclopedia

remains unparalleled in its size and in the breadth of topicsand organisms it covers

The revision of these volumes could not come at a moreopportune time In fact, there is a desperate need for a deeperunderstanding and appreciation of our natural world Manyspecies are classified as threatened or endangered, and the sit-uation is expected to get much worse before it gets better.Species extinction has always been part of the evolutionaryhistory of life; some organisms adapt to changing circum-stances and some do not However, the current rate of speciesloss is now estimated to be 1,000–10,000 times the normal

“background” rate of extinction since life began on Earthsome 4 billion years ago The primary factor responsible forthis decline in biological diversity is the exponential growth

of human populations, combined with peoples’ unsustainableappetite for natural resources, such as land, water, minerals,oil, and timber The world’s human population now exceeds

6 billion, and even though the average birth rate has begun

to decline, most demographers believe that the global humanpopulation will reach 8–10 billion in the next 50 years Much

of this projected growth will occur in developing countries inCentral and South America, Asia and Africa—regions that arerich in unique biological diversity

• • • • •

Foreword

Finding solutions to conservation challenges will not be

easy in today’s human-dominated world A growing number

of people live in urban settings and are becoming increasingly

isolated from nature They “hunt” in supermarkets and malls,

live in apartments and houses, spend their time watching

tele-vision and searching the World Wide Web Children and

adults must be taught to value biological diversity and the

habitats that support it Education is of prime importance now

while we still have time to respond to the impending crisis

There still exist in many parts of the world large numbers of

biological “hotspots”—places that are relatively unaffected by

humans and which still contain a rich store of their original

animal and plant life These living repositories, along with

se-lected populations of animals and plants held in

profession-ally managed zoos, aquariums and botanical gardens, could

provide the basis for restoring the planet’s biological wealth

and ecological health This encyclopedia and the collective

knowledge it represents can assist in educating people about

animals and their ecological and cultural significance Perhaps

it will also assist others in making deeper connections to

na-ture and spreading biophilia Information on the

conserva-tion status, threats and efforts to preserve various species have

been integrated into this revision We have also included

in-formation on the cultural significance of animals, including

their roles in art and religion

It was over 30 years ago that Dr Bernhard Grzimek, then

director of the Frankfurt Zoo in Frankfurt, Germany, edited

the first edition of Grzimek’s Animal Life Encyclopedia Dr

Grz-imek was among the world’s best known zoo directors and

conservationists He was a prolific author, publishing nine

books Among his contributions were: Serengeti Shall Not Die,

Rhinos Belong to Everybody and He and I and the Elephants Dr.

Grzimek’s career was remarkable He was one of the first

modern zoo or aquarium directors to understand the

impor-tance of zoo involvement in in situ conservation, that is, of

their role in preserving wildlife in nature During his tenure,

Frankfurt Zoo became one of the leading western advocates

and supporters of wildlife conservation in East Africa Dr

Grzimek served as a Trustee of the National Parks Board of

Uganda and Tanzania and assisted in the development of

sev-eral protected areas The film he made with his son Michael,

Serengeti Shall Not Die, won the 1959 Oscar for best

docu-mentary

Professor Grzimek has recently been criticized by some

for his failure to consider the human element in wildlife

con-servation He once wrote: “A national park must remain a

pri-mordial wilderness to be effective No men, not even native

ones, should live inside its borders.” Such ideas, although

con-sidered politically incorrect by many, may in retrospect

actu-ally prove to be true Human populations throughout Africa

continue to grow exponentially, forcing wildlife into small

is-lands of natural habitat surrounded by a sea of humanity The

illegal commercial bushmeat trade—the hunting of

endan-gered wild animals for large scale human consumption—is

pushing many species, including our closest relatives, the

go-rillas, bonobos and chimpanzees, to the brink of extinction

The trade is driven by widespread poverty and lack of

eco-nomic alternatives In order for some species to survive it will

be necessary, as Grzimek suggested, to establish and enforce

a system of protected areas where wildlife can roam free fromexploitation of any kind

While it is clear that modern conservation must take theneeds of both wildlife and people into consideration, what willthe quality of human life be if the collective impact of short-term economic decisions is allowed to drive wildlife popula-tions into irreversible extinction? Many rural populations living

in areas of high biodiversity are dependent on wild animals astheir major source of protein In addition, wildlife tourism isthe primary source of foreign currency in many developingcountries and is critical to their financial and social stability.When this source of protein and income is gone, what will be-come of the local people? The loss of species is not only a con-servation disaster; it also has the potential to be a human tragedy

of immense proportions Protected areas, such as nationalparks, and regulated hunting in areas outside of parks are theonly solutions What critics do not realize is that the fate ofwildlife and people in developing countries is closely inter-twined Forests and savannas emptied of wildlife will result inhungry, desperate people, and will, in the long-term lead to ex-treme poverty and social instability Dr Grzimek’s early con-tributions to conservation should be recognized, not only asbenefiting wildlife, but as benefiting local people as well

Dr Grzimek’s hope in publishing his Animal Life

Encyclo-pedia was that it would “ disseminate knowledge of the

ani-mals and love for them”, so that future generations would

“ have an opportunity to live together with the great sity of these magnificent creatures.” As stated above, our goals

diver-in producdiver-ing this updated and revised edition are similar.However, our challenges in producing this encyclopedia weremore formidable The volume of knowledge to be summa-rized is certainly much greater in the twenty-first century than

it was in the 1970’s and 80’s Scientists, both professional andamateur, have learned and published a great deal about theanimal kingdom in the past three decades, and our under-standing of biological and ecological theory has also pro-gressed Perhaps our greatest hurdle in producing this revisionwas to include the new information, while at the same time

retaining some of the characteristics that have made Grzimek’s

Animal Life Encyclopedia so popular We have therefore strived

to retain the series’ narrative style, while giving the

informa-tion more organizainforma-tional structure Unlike the original

Grz-imek’s, this updated version organizes information under

specific topic areas, such as reproduction, behavior, ecologyand so forth In addition, the basic organizational structure isgenerally consistent from one volume to the next, regardless

of the animal groups covered This should make it easier forusers to locate information more quickly and efficiently Likethe original Grzimek’s, we have done our best to avoid anyoverly technical language that would make the work difficult

to understand by non-biologists When certain technical pressions were necessary, we have included explanations orclarifications

ex-Considering the vast array of knowledge that such a workrepresents, it would be impossible for any one zoologist tohave completed these volumes We have therefore sought spe-cialists from various disciplines to write the sections with

which they are most familiar As with the original Grzimek’s,

we have engaged the best scholars available to serve as topic

editors, writers, and consultants There were some complaints

about inaccuracies in the original English version that may

have been due to mistakes or misinterpretation during the

complicated translation process However, unlike the

origi-nal Grzimek’s, which was translated from German, this

revi-sion has been completely re-written by English-speaking

scientists This work was truly a cooperative endeavor, and I

thank all of those dedicated individuals who have written,

edited, consulted, drawn, photographed, or contributed to its

production in any way The names of the topic editors,

au-thors, and illustrators are presented in the list of contributors

in each individual volume

The overall structure of this reference work is based on

the classification of animals into naturally related groups, a

discipline known as taxonomy or biosystematics Taxonomy

is the science through which various organisms are

discov-ered, identified, described, named, classified and catalogued

It should be noted that in preparing this volume we adopted

what might be termed a conservative approach, relying

pri-marily on traditional animal classification schemes

Taxon-omy has always been a volatile field, with frequent arguments

over the naming of or evolutionary relationships between

var-ious organisms The advent of DNA fingerprinting and other

advanced biochemical techniques has revolutionized the field

and, not unexpectedly, has produced both advances and

con-fusion In producing these volumes, we have consulted with

specialists to obtain the most up-to-date information

possi-ble, but knowing that new findings may result in changes at

any time When scientific controversy over the classification

of a particular animal or group of animals existed, we did our

best to point this out in the text

Readers should note that it was impossible to include as

much detail on some animal groups as was provided on

oth-ers For example, the marine and freshwater fish, with vast

numbers of orders, families, and species, did not receive as

detailed a treatment as did the birds and mammals Due topractical and financial considerations, the publishers couldprovide only so much space for each animal group In suchcases, it was impossible to provide more than a broad overviewand to feature a few selected examples for the purposes of il-lustration To help compensate, we have provided a few keybibliographic references in each section to aid those inter-ested in learning more This is a common limitation in all ref-

erence works, but Grzimek’s Encyclopedia of Animal Life is still

the most comprehensive work of its kind

I am indebted to the Gale Group, Inc and Senior EditorDonna Olendorf for selecting me as Series Editor for this pro-ject It was an honor to follow in the footsteps of Dr Grz-imek and to play a key role in the revision that still bears his

name Grzimek’s Animal Life Encyclopedia is being published

by the Gale Group, Inc in affiliation with my employer, theAmerican Zoo and Aquarium Association (AZA), and I wouldlike to thank AZA Executive Director, Sydney J Butler; AZAPast-President Ted Beattie (John G Shedd Aquarium,Chicago, IL); and current AZA President, John Lewis (JohnBall Zoological Garden, Grand Rapids, MI), for approving

my participation I would also like to thank AZA tion and Science Department Program Assistant, MichaelSouza, for his assistance during the project The AZA is a pro-fessional membership association, representing 215 accred-ited zoological parks and aquariums in North America AsDirector/William Conway Chair, AZA Department of Con-servation and Science, I feel that I am a philosophical de-scendant of Dr Grzimek, whose many works I have collectedand read The zoo and aquarium profession has come a longway since the 1970s, due, in part, to innovative thinkers such

Conserva-as Dr Grzimek I hope this latest revision of his work willcontinue his extraordinary legacy

Silver Spring, Maryland, 2001

Michael Hutchins

Series Editor

Grzimek’s Animal Life Encyclopedia is an internationally

prominent scientific reference compilation, first published in

German in the late 1960s, under the editorship of zoologist

Bernhard Grzimek (1909–1987) In a cooperative effort

be-tween Gale and the American Zoo and Aquarium Association,

the series has been completely revised and updated for the

first time in over 30 years Gale expanded the series from 13

to 17 volumes, commissioned new color paintings, and

up-dated the information so as to make the set easier to use The

order of revisions is:

Volumes 8–11: Birds I–IV

Volume 6: Amphibians

Volume 7: Reptiles

Volumes 4–5: Fishes I–II

Volumes 12–16: Mammals I–V

Volume 3: Insects

Volume 2: Protostomes

Volume 1: Lower Metazoans and Lesser Deuterostomes

Volume 17: Cumulative Index

Organized by taxonomy

The overall structure of this reference work is based on

the classification of animals into naturally related groups, a

discipline known as taxonomy—the science in which various

organisms are discovered, identified, described, named,

clas-sified, and catalogued Starting with the simplest life forms,

the lower metazoans and lesser deuterostomes, in volume 1,

the series progresses through the more complex classes of

an-imals, culminating with the mammals in volumes 12–16

Vol-ume 17 is a stand-alone cumulative index

Organization of chapters within each volume reinforces

the taxonomic hierarchy In the case of the volume on

Pro-tostomes, introductory chapters describe general

characteris-tics of all organisms in these groups, followed by taxonomic

chapters dedicated to Phylum, Class, Subclass, or Order

Species accounts appear at the end of the taxonomic chapters

To help the reader grasp the scientific arrangement, each type

of chapter has a distinctive color and symbol:

■ = Phylum Chapter (lavender background)

¢ = Class Chapter (peach background)

= Subclass Chapter (peach background)

● = Order Chapter (blue background)Introductory chapters have a loose structure, reminiscent

of the first edition Chapters on taxonomic groups, by trast, are highly structured, following a prescribed format ofstandard rubrics that make information easy to find Thesechapters typically include:

con-Opening sectionScientific nameCommon namePhylumClass (if applicable)Subclass (if applicable)Order (if applicable)Number of familiesThumbnail descriptionMain chapter

Evolution and systematicsPhysical characteristicsDistribution

HabitatBehaviorFeeding ecology and dietReproductive biologyConservation statusSignificance to humansSpecies accountsCommon nameScientific nameOrder (if applicable)Family

TaxonomyOther common namesPhysical characteristicsDistribution

HabitatBehaviorFeeding ecology and dietReproductive biologyConservation statusSignificance to humans

• • • • •

How to use this book

Color graphics enhance understanding

Grzimek’s features approximately 3,000 color photos,

in-cluding nearly 110 in the Protostomes volume; 3,500 total

color maps, including approximately 115 in the Protostomes

volume; and approximately 5,500 total color illustrations,

in-cluding approximately 280 in the Protostomes volume Each

featured species of animal is accompanied by both a

distrib-ution map and an illustration

All maps in Grzimek’s were created specifically for the

ject by XNR Productions Distribution information was

pro-vided by expert contributors and, if necessary, further

researched at the University of Michigan Zoological Museum

library Maps are intended to show broad distribution, not

definitive ranges

All the color illustrations in Grzimek’s were created

specif-ically for the project by Michigan Science Art Expert

con-tributors recommended the species to be illustrated and

provided feedback to the artists, who supplemented this

in-formation with authoritative references and animal specimens

from the University of Michigan Zoological Museum library

In addition to illustrations of species, Grzimek’s features

draw-ings that illustrate characteristic traits and behaviors

About the contributors

Virtually all of the chapters were written by scientists who

are specialists on specific subjects and/or taxonomic groups

Sean F Craig reviewed the completed chapters to insure

con-sistency and accuracy

Standards employed

In preparing the volume on Protostomes, the editors relied

primarily on the taxonomic structure outlined in Invertebrates,

edited by R C Brusca, and G J Brusca (1990) Systematics is

a dynamic discipline in that new species are being discovered

continuously, and new techniques (e.g., DNA sequencing)

fre-quently result in changes in the hypothesized evolutionary

relationships among various organisms Consequently,

contro-versy often exists regarding classification of a particular animal

or group of animals; such differences are mentioned in the text

Readers should note that even though insects are protostomes,

they are treated in a separate volume (Volume 3)

Grzimek’s has been designed with ready reference in mind,

and the editors have standardized information wherever

fea-sible For Conservation Status, Grzimek’s follows the IUCN

Red List system, developed by its Species Survival

Commis-sion The Red List provides the world’s most comprehensive

inventory of the global conservation status of plants and

ani-mals Using a set of criteria to evaluate extinction risk, the

IUCN recognizes the following categories: Extinct, Extinct inthe Wild, Critically Endangered, Endangered, Vulnerable,Conservation Dependent, Near Threatened, Least Concern,and Data Deficient For a complete explanation of each cate-gory, visit the IUCN web page at <http://www.iucn.org/themes/ssc/redlists/categor.htm>

In addition to IUCN ratings, chapters may contain otherconservation information, such as a species’ inclusion on one

of three Convention on International Trade in EndangeredSpecies (CITES) appendices Adopted in 1975, CITES is aglobal treaty whose focus is the protection of plant and ani-mal species from unregulated international trade

In the Species accounts throughout the volume, the editorshave attempted to provide common names not only in Eng-lish but also in French, German, Spanish, and local dialects

Grzimek’s provides the following standard information on

lineage in the Taxonomy rubric of each Species account:

[First described as] Epimenia australis [by] Thiele, [in] 1897,

[based on a specimen from] Timor Sea, at a depth of 590 ft(180 m) The person’s name and date refer to earliest identi-fication of a species If the species was originally describedwith a different scientific name, the researcher’s name and thedate are in parentheses

Readers should note that within chapters, species accountsare organized alphabetically by order name, then by family,and then by genus and species

fined in the Glossary at the back of the book.

Appendices and index

In addition to the main text and the aforementioned

Glos-sary, the volume contains numerous other elements For ther reading directs readers to additional sources of

fur-information about protostomes Valuable contact fur-information

for Organizations is also included in an appendix An haustive Protostomes family list records all orders of pro-

ex-tostomes as recognized by the editors and contributors of the

volume And a full-color Geologic time scale helps readers

understand prehistoric time periods Additionally, the volume

contains a Subject index.

volume, oversaw all phases of the volume, including creation

of the topic list, chapter review, and compilation of the

ap-pendices Neil Schlager, project manager for the Protostomes

volume, and Vanessa Torrado-Caputo, associate editor at

Schlager Group, coordinated the writing and editing of the

text Dr Michael Hutchins, chief consulting editor for the ries, and Michael Souza, program assistant, Department ofConservation and Science at the American Zoo and Aquar-ium Association, provided valuable input and research sup-port

se-Series advisor

Michael Hutchins, PhD

Director of Conservation and Science/William Conway

Chair

American Zoo and Aquarium Association

Silver Spring, Maryland

Subject advisors

Volume 1: Lower Metazoans and Lesser Deuterostomes

Dennis A Thoney, PhD

Director, Marine Laboratory & Facilities

Humboldt State University

Arcata, California

Volume 2: Protostomes

Sean F Craig, PhD

Assistant Professor, Department of Biological Sciences

Humboldt State University

Arcata, California

Dennis A Thoney, PhD

Director, Marine Laboratory & Facilities

Humboldt State University

Research Associate, Department of Entomology

Natural History Museum

Los Angeles, California

Volumes 4–5: Fishes I– II

Paul V Loiselle, PhD

Curator, Freshwater Fishes

New York Aquarium

Brooklyn, New YorkDennis A Thoney, PhDDirector, Marine Laboratory & FacilitiesHumboldt State University

Arcata, California

Volume 6: Amphibians

William E Duellman, PhDCurator of Herpetology EmeritusNatural History Museum and Biodiversity Research CenterUniversity of Kansas

Lawrence, Kansas

Volume 7: Reptiles

James B Murphy, DScSmithsonian Research AssociateDepartment of HerpetologyNational Zoological ParkWashington, DC

Volumes 8–11: Birds I–IV

Walter J Bock, PhDPermanent secretary, International Ornithological CongressProfessor of Evolutionary Biology

Department of Biological Sciences,Columbia University

New York, New YorkJerome A Jackson, PhDProgram Director, Whitaker Center for Science, Mathematics, and Technology EducationFlorida Gulf Coast University

Ft Myers, Florida

Volumes 12–16: Mammals I–V

Valerius Geist, PhDProfessor Emeritus of Environmental ScienceUniversity of Calgary

Calgary, AlbertaCanada

• • • • •

Advisory boards

Devra G Kleiman, PhD

Smithsonian Research Associate

National Zoological Park

Washington, DC

Library advisors

James Bobick

Head, Science & Technology Department

Carnegie Library of Pittsburgh

Pittsburgh, Pennsylvania

Linda L Coates

Associate Director of Libraries

Zoological Society of San Diego Library

San Diego, California

Lloyd Davidson, PhD

Life Sciences bibliographer and head, Access Services

Seeley G Mudd Library for Science and Engineering

Library Media SpecialistPlymouth Salem High SchoolPlymouth, Michigan

Ken KisterReviewer/General Reference teacherTampa, Florida

Richard NaglerReference LibrarianOakland Community CollegeSouthfield Campus

Southfield, MichiganRoland PersonLibrarian, Science DivisionMorris Library

Southern Illinois UniversityCarbondale, Illinois

Charles I Abramson, PhD

Oklahoma State University

Stillwater, Oklahoma

Tatiana Amabile de Campos, MSc

Universidade Estadual de Campinas

Campinas, Brazil

Alberto Arab, PhD

William Arthur Atkins

Atkins Research and Consulting

The Natural History Museum

London, United Kingdom

Sherri Chasin Calvo

Independent Science Writer

Peter B Mordan, PhDThe Natural History MuseumLondon, United KingdomPaulo Ricardo Nucci, PhDUniversidade Estadual de CampinasCampinas, Brazil

Erica Veronica Pardo, PhDAmanda Louise Reid, PhDBulli, Australia

Patrick D Reynolds, PhDHamilton College

Clinton, New YorkJohn Riley, PhDUniversity of DundeeDundee, ScotlandJohana Rincones, PhDUniversidade Estadual de CampinasCampinas, Brazil

Greg W Rouse, PhDSouth Australian MuseumAdelaide, AustraliaMichael S Schaadt, MSCabrillo Marine AquariumSan Pedro, CaliforniaUlf Scheller, PhDJarpas, SwedenHorst Kurt Schminke, PhDCarl von Ossietzky Universität Olden-burg

Oldenburg, Germany

Kevin F Fitzgerald, BSIndependent Science WriterSteven Mark Freeman, PhDABP Marine Environmental ResearchLtd

Southampton, United KingdomRick Hochberg, PhD

Smithsonian Marine Station at FortPierce

Fort Pierce, FloridaSamuel Wooster James, PhDUniversity of Kansas

Lawrence, KansasGregory C Jensen, PhDUniversity of WashingtonSeattle, WashingtonReinhardt Møbjerg Kristensen, PhDZoological Museum

University of CopenhagenCopenhagen, DenmarkDavid Lindberg, PhDMuseum of PaleontologyUniversity of California, BerkeleyBerkeley, California

Estela C Lopretto, PhDMuseo de La PlataBuenos Aires, ArgentinaTatiana Menchini Steiner, PhDUniversidade Estadual de CampinasCampinas, Brazil

Leslie Ann Mertz, PhDWayne State UniversityDetroit, MichiganPaula M Mikkelsen, PhDAmerican Museum of Natural HistoryNew York, New York

• • • • •

Contributing writers

Anja Schulze, PhD

Harvard University

Cambridge, Massachusetts

Mark Edward Siddall, PhD

American Museum of Natural History

New York, New York

Martin Vinther Sørensen, PhD

Zoological Museum

University of Copenhagen

Copenhagen, Denmark

Eve C Southward, PhD, DSc

Marine Biological Association

Plymouth, United Kingdom

Tatiana Menchini Steiner, PhDUniversidade Estadual de CampinasSão Paulo, Brazil

Per A Sundberg, PhDGöteborg UniversityGöteborg, SwedenMichael Vecchione, PhDNational Museum of Natural HistoryWashington, DC

Les Watling, PhDUniversity of MaineDarling Marine Center

Walpole, MaineTim Wood, PhDWright State UniversityDayton, Ohio

Jill Yager, PhDAntioch CollegeYellow Springs, Ohio

Drawings by Michigan Science Art

Joseph E Trumpey, Director, AB, MFA

Science Illustration, School of Art and Design, University

of Michigan

Wendy Baker, ADN, BFA

Ryan Burkhalter, BFA, MFA

Brian Cressman, BFA, MFA

Emily S Damstra, BFA, MFA

Maggie Dongvillo, BFA

Barbara Duperron, BFA, MFA

Jarrod Erdody, BA, MFA

Dan Erickson, BA, MS

Patricia Ferrer, AB, BFA, MFA

George Starr Hammond, BA, MS, PhD

Gillian Harris, BA

Jonathan Higgins, BFA, MFAAmanda Humphrey, BFAEmilia Kwiatkowski, BS, BFAJacqueline Mahannah, BFA, MFAJohn Megahan, BA, BS, MSMichelle L Meneghini, BFA, MFAKatie Nealis, BFA

Laura E Pabst, BFAAmanda Smith, BFA, MFAChristina St.Clair, BFABruce D Worden, BFAKristen Workman, BFA, MFA

Thanks are due to the University of Michigan, Museum of Zoology, which provided specimens that served as models for the images.

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Topic overviews

What is a protostome?

Evolution and systematics

Reproduction, development, and life history

Ecology Symbiosis Behavior Protostomes and humans

• • • • •

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Origin of Protostomia

The term Protostomia (from the Greek “proto,” meaning

first, and “stoma,” meaning mouth) was coined by the

biolo-gist Karl Grobben in 1908 It distinguishes a group of

inver-tebrate animals based upon the fate of the blastopore (the first

opening of the early digestive tract) during embryonic

devel-opment Animals in which the blastopore becomes the mouth

are called protostomes; those in which the mouth develops

after the anus are called deuterostomes (from the Greek

“deutero,” meaning second, and “stoma,” meaning mouth)

Protostomia and Deuterostomia are considered

super-phyletic taxa, each containing a variety of animal phyla

Tra-ditionally, the protostomes include the Annelida, Arthropoda,

and Mollusca, and the deuterostomes comprise the

Echino-dermata and Chordata Grobben was not the first biologist to

recognize the distinction between these two groups, but he

was the first to place importance on the fate of the blastopore

as a major distinguishing criterion Historically, the two

groups are distinguished by the following criteria:

1 Embryonic cleavage pattern (that is, how the

zy-gote divides to become a multicellular animal)

2 Fate of the blastopore

3 Origin of mesoderm (the “middle” embryonic

tis-sue layer between ectoderm and endoderm that

forms various structures such as muscles and

skeleton)

4 Method of coelom formation

5 Type of larva

These developmental features are different in the two

groups and can be summarized as follows:

Developmental features of protostomes

1 Cleavage pattern: spiral cleavage

2 Fate of blastopore: becomes the mouth

3 Origin of mesoderm arises from mesentoblast

(4d cells)

4 Coelom formation: schizocoely

5 Larval type: trochophore larva

Developmental features of deuterostomes

1 Cleavage pattern: radial cleavage

2 Fate of blastopore: becomes the anus

3 Origin of mesoderm: pouches off gut (endoderm)

4 Coelom formation: enterocoely

5 Larval type: dipleurulaCleavage pattern refers to the process of cell division fromone fertilized cell, the zygote, into hundreds of cells, the em-bryo In protostomes, the developing zygote undergoes spi-ral cleavage, a process in which the cells divide at a 45° angle

to one another due to a realignment of the mitotic spindle.The realignment of the mitotic spindle causes each cell to di-vide unequally, resulting in a spiral displacement of small cells,the micromeres, that come to sit atop the border betweenlarger cells, the macromeres Another superphyletic term used

to describe animals with spiral cleavage is Spiralia Spiralcleavage is also called determinate cleavage, because the func-tion of the cells is determined early in the cleavage process.The removal of any cell from the developing embryo will re-sult in abnormal development, and individually removed cellswill not develop into complete larvae

In deuterostomes, the zygote undergoes radial cleavage, aprocess in which the cells divide at right angles to one an-other Radial cleavage is also known as indeterminate cleav-age, because the fate of the cells is not fixed early indevelopment The removal of a single cell from a developingembryo will not cause abnormal development, and individu-ally removed cells can develop into complete larvae, produc-ing identical twins, triplets, and so forth

The fate of the blastopore has classically been used as thedefining characteristic of protostomes and deuterostomes Inprotostomes, the blastopore develops into the mouth, and theanus develops from an opening later in development Indeuterostomes, the blastopore develops into the anus, and themouth develops secondarily

Mesoderm and coelom formation are intimately tied gether during development In protostomes, the mesodermoriginates from a pair of cells called mesentoblasts (also called

to-• to-• to-• to-• to-•

What is a protostome?

4d cells) next to the blastopore, which then migrate into the

blastocoel, the internal cavity of the embryo, to become

var-ious internal structures In coelomates, the mesentoblasts

hol-low out to become coeloms, cavities lined by a contractile

peritoneum, the myoepithelium In protostomes, the process

of coelom formation is called schizocoely In deuterostomes,

the mesoderm originates from the wall of the archenteron, an

early digestive tract formed from endoderm The archenteron

pouches out to form coelomic cavities, in a process called

en-terocoely

Protostomia and Deuterostomia are also characterized by

different larvae In most protostomes, the larval type is a

tro-chophore, basically defined by the presence of two rings of

multiciliated cells (prototroch and metatroch) surrounding a

ciliated zone around the mouth Most deuterostomes have a

dipleurula-type larva, defined by the presence of a field of cilia

(monociliated cells) surrounding the mouth

Contemporary reexamination of Protostomia

For more than a century, biologists have divided the

bilateral animals into two main lineages (the diphyletic

origin of Bilateria), the most well known of which is the

Protostomia/Deuterostomia split Similar divisions includethe Zygoneura/Ambulacralia-Chordonia split proposed bythe German invertebrate embryologist Hatschek in 1888, theHyponeuralia/Epineuralia split proposed by the French zo-ologist Cuenot in 1940, and a Gastroneuralia/Notoneuraliasplit proposed by the German zoologist Ulrich in 1951,among others These divisions often emphasized different de-velopmental and adult features, thereby leading to differentnames and hypotheses about animal relationships Althoughnone of these groups have been granted formal taxonomicrank (for example, as a subkingdom or superphylum) by theInternational Code of Zoological Nomenclature, the namesnevertheless remain active in the literature

Contemporary research on protostome relationships lizes a host of methods and technologies that were unavail-able to biologists in the early twentieth century, such asGrobben Modern biologists employ electron microscopy,fluorescent microscopy, biochemistry, and a collection ofmolecular techniques to sequence the genome, trace embry-onic development, and gain insight into the origin of various

uti-genes and gene clusters, such as Hox uti-genes Other fields of

research, including cladistic analysis and bioinformatics, tinue to make important contributions The latter fields arecomputer-based technologies that employ algorithms and sta-

con-Protostomes have exoskeletons When they grow, they shed their outer layer (Photo by A Captain/R Kulkarni/S Thakur Reproduced by mission.)

per-tistics to handle and analyze large data sets, such as lists of

morphological characters and nucleotide sequences Together

with new paleontological discoveries in the fossil realm, these

novel techniques and technologies provide modern biologists

with a useful way to reexamine the traditional protostome

re-lationships and to develop new hypotheses on animal

rela-tionships and evolution

With the arrival of new information and a more

encom-passing examination of all the animal phyla, the modern view

of Protostomia has broadened from that originally proposed by

Grobben, which, at one time or another, included the

follow-ing phyla: Brachiopoda, Chaetognatha, Cycliophora,

Ecto-procta, EntoEcto-procta, Echiura, Gastrotricha, Gnathostomulida,

Kinorhyncha, Loricifera, Nemertinea, Nematoda,

Nemato-morpha, Onychophora, Phoronida, Platyhelminthes,

Priapul-ida, Rotifera, Sipuncula, and Tardigrada Many of these phyla

contain species that display one or more developmental

char-acters outlined by Grobben; however, it is rare to find more

than a handful of species from any phylum that meet all thetraditional protostome criteria Questions have been raisedabout their relationships, even among “typical” protostomessuch as arthropods For example, the only known arthropodswith typical spiral cleavage are the cirripede crustaceans (bar-

nacles such as Balanus balanoides) and some primitive

chelicer-ates (such as horseshoe crabs and spiders), and these are but afew compared to the millions of species in the phylum More-over, some phyla, such as Ectoprocta, Nematomorpha, and Pri-apulida, share no developmental characters with the typicalprotostome, and for others, such as Gnathostomulida and Lori-cifera, very little developmental information exists This hascalled into question the validity of the Protostomia as a nat-ural, monophyletic group In fact, whether or not Protostomia

is accepted by biologists as monophyletic often depends uponthe type of data collected, such as molecular sequences, em-bryology, and morphology, and how the data are analyzed.The evolutionary origin of the Protostomia, and of thegroups it includes, remains a major challenge to modern bi-ologists Although proof of the monophyly of the Protosto-mia is elusive, many of the phyla are clearly related, and make

up clades that some biologists consider monophyletic For ample, in 1997 Aguinaldo et al proposed the establishment

ex-of two clades within the Protostomia based on molecular quence data: Ecdysozoa (the molting animals, including theArthropoda, Nematoda, Priapulida, and Tardigrada), andLophotrochozoa (the ciliated animals, including the Annel-ida, Echiura, and Sipuncula) Biologists continue to debatethese hypotheses and test them with independent biochemi-cal, developmental, molecular, and morphological data

se-A fire worm (Eurythoe complanata) with vemonous bristles (Photo by

A Flowers & L Newman Reproduced by permission.)

A land snail crawling on grass (Photo by JLM Visuals Reproduced by permission.)

Books

Brusca, R C., and G J Brusca Invertebrates, 2nd ed New

York: Sinauer Associates, 2003

Nielsen, C Animal Evolution: Interrelationships of the Living

Phyla, 2nd ed New York: Oxford University Press, 2001.

Periodicals

Aguinaldo, A M A., et al “Evidence for a Clade of

Nematodes, Arthropods and Other Moulting Animals.”

Nature 387 (1997): 483–491.

Løvtrup, S “Validity of the Protostomia-Deuterostomia

Theory.” Systematic Zoology 24 (1975): 96–108.

Winnepenninckx, B., T Backeljau, L Y Mackey, J M.Brooks, R de Wachter, S Kumar, and J R Garey

“Phylogeny of Protostome Worms Derived from 18S rRNA

Sequences.” Molecular Biology and Evolution 12 (1995):

641–649

Rick Hochberg, PhD

Roots and methods of systematics and

classification

There is only one figure in the 1859 first edition of Charles

Darwin’s On the Origin of Species; it is what biologists now call

a phylogenetic tree A phylogenetic tree is a diagram that

shows how animals have evolved from a common ancestor by

branching out from it Darwin himself did not use the term

“phylogeny,” but he referred to his tree as a “diagram of

di-vergence of taxa.” Darwin wrote primarily about evolution in

Origin, but he devoted parts of Chapter XIII to classification,

in which he gave a clear account of what he considered a

nat-ural system for classifying organisms: “I hold the natnat-ural

sys-tem is genealogical in its arrangement, like a pedigree; but

the degrees of modification which the different groups have

undergone, have to be expressed by ranking them under

dif-ferent so-called genera, sub-families, families, sections,

or-ders, and classes.” The science of systematics, which includes

taxonomy, is the oldest and most encompassing of all fields

of biology, and in 1859 natural history was largely a matter

of classifying Darwin’s statement may not sound particularly

revolutionary to modern adherents of the theory of evolution;

however, biological classification before the mid-nineteenth

century had essentially been a matter of imposing some kind

of order on a complex nature created by God (Obviously,

classifications at that time did not reflect any underlying

process simply because the process of evolution was unknown

then.) Darwin’s concept quickly won acceptance among

biol-ogists, and phylogenetic trees became the standard way to

de-pict the evolution of recent taxa and how taxa have originated

from a common ancestor

If scientists wish to classify living animals to reflect their

evolutionary relationships, they must first investigate the

phy-logeny of the organisms in question Darwin did not devise a

method for determining phylogenetic relationships other than

in very general terms, however Although phylogenies began

to appear in the late nineteenth century, they were based on

subjective assessments of the morphological similarities and

differences that were then regarded as indications of kinship

Even though many authors have used phylogenetic terms in

discussing their systems of classification, one must bear in

mind that many of the classifications found in textbooks are

not based on any explicit phylogenetic analysis In fact, it was

not until the mid-twentieth century that theoretical as well as

methodological advances in the field of systematics led gists to better supported phylogenetic hypotheses As of 2003,most systematists and evolutionary biologists use these meth-ods, which are known as phylogenetic systematics or cladis-tics, to infer relationships among various animals and presentthe results in the form of a cladogram or phylogenetic tree.The basic concept in phylogenetic systematics is mono-phyly A monophyletic group of species is one that includesthe ancestral species and all of its descendants Thus, a mono-phyletic taxon is a group of species whose members are re-lated to one another through a shared history of descent; that

biolo-is, a single evolutionary lineage There are several taxa andnames still in use that are not monophyletic; some have sur-vived because they are still in common use—for example, “in-vertebrates”—and others because we know little about theirevolutionary history The basis for determining evolutionaryrelationships is homology, a term that refers to similarities re-sulting from shared ancestry The cladistic term for this sim-ilarity is synapomorphy It is these homologous charactersthat point to a common ancestry For example, the presence

of a backbone in birds, lizards and humans indicates that thesethree groups share a common ancestor and are thus related.Similarity, however, does not always reflect common ances-try; sometimes it points to convergent evolution The ad-vanced octopus eye, which in many ways resembles the humaneye, is not an indication of a relationship between octopodsand humans Cladistic methods are used to distinguish be-tween similarities resulting from a common ancestry and sim-ilarities due to other causes

In the past, biologists used morphological characters as theprimary source for investigating relationships Most of thecurrent taxonomic classification is based on assessment ofmorphological similarities and differences Morphologicalcharacters alone, however, have obvious limitations in deter-mining phylogeny within the animal kingdom It is difficult

to find similarities between, say, a flatworm and a sponge ifthe researcher must rely on gross morphology and anatomy.Some taxonomists therefore turned to embryological charac-teristics; many relationships among animals have been estab-lished on the basis of sperm morphology or larval biology.The advent of polymerase chain reaction (PCR) technologyand direct nucleotide sequencing has brought about immensechanges in the amount of information available for phylogeny

• • • • •

Evolution and systematics

evaluation The finding that animals at all levels share large

portions of the genome makes it possible to compare taxa as

far apart as vertebrates and nematodes at homologous gene

loci Biologists can feel confident that they are comparing the

“same” thing when they look at the base composition of a

gene such as 18s rDNA, because there are so many overall

genetic similarities in this gene between taxa A staggering

amount of new information has been collected from DNA;

at present, all new gene sequences are deposited in banks like

GenBank, which makes them available to the worldwide

sci-entific community Researchers are thus getting closer to

finding the actual Tree of Life; electronic databases and

in-formation sharing have led them much closer to realizing

Darwin’s vision of a classification based on genealogy On the

other hand, these recent advances mean that many traditional

views of relationships among various groups of animals are

open to question It is not easy to write about metazoan

phy-logeny today, knowing that so many established “truths” have

already been overturned, and more will certainly be

chal-lenged in the near future

As of 2003, the classification of animals is defined by the

International Code of Zoological Nomenclature, established

on January 1, 1758—the year of publication of the tenth

edi-tion of Linnaeus’s Systema Naturae This code regulates the

naming of species, genera, and families It states that a species

name should refer to a holotype, which is a designated

spec-imen deposited in a museum or similar institution In theory,

the holotype should be available to anyone who wishes to study

it The genus is defined by the type (typical) species, and the

family name is defined by the type genus Although the

con-vention has developed of using a series of hierarchical

cate-gories, these other ranks are not covered by the code and are

not defined in the same explicit way The most inclusive

cat-egory is kingdom, followed by phylum Although phyla are

not formally defined in the Code, and authors disagree about

their definition in some instances, “phylum” is probably the

category most easily recognized by nonspecialists Members

of a phylum have a similar baüplan (the German word for an

architect’s ground plan for a building) or body organization,

and share some obvious synapomorphies, or specialized

char-acters that originated in the last common ancestor These

sim-ilarities and shared characters are not always obvious, however;

the rank of phylum for some taxa is open to debate

Molecu-lar data have also challenged the monophyletic status of some

phyla that were previously unquestioned It is evident that the

cladistic approach to systematics, combined with an ever

in-creasing amount of data from molecular genetics, has ushered

in a period of taxonomic turmoil

Kingdoms of life

The world of living organisms can be divided into two

ma-jor groups, the prokaryotes and the eukaryotes The

prokary-otes lack membrane-enclosed organelles and a nucleus, while

the eukaryotes do possess organelles and a nucleus inside their

membranes, and have linear chromosomes (By 2003,

how-ever, an organelle was found in a bacterium—which overturns

the assumption that these specialized compartments are

unique to the eukaryotes.) The prokaryotes have been

subdi-vided into two kingdoms: Eubacteria (bacteria) and Archea(archaebacteria) The eukaryotic kingdom has been subdi-vided into the Animalia or Metazoa and the “animal-like or-ganisms” or Protozoa As of 2003, however, the protozoansare most often referred to as the Kingdom Protista; that is,eukaryotic single-celled microorganisms together with certainalgae This kingdom contains around 18 phyla that includeamoebas, dinoflagellates, foraminiferans and ciliates King-dom Animalia contains about 34 phyla of heterotrophic mul-ticellular organisms The number is approximate becausethere is currently no consensus regarding the detailed classi-fication of taxa into phyla About 1.3 million living specieshave been described, but this number is undoubtedly an un-derestimate Estimates of undescribed species range from lows

of 10–30 million to highs of 100–200 million

The beginnings of life

Clearly the prokaryotes are the most ancient living isms, but when did they first appear? There is indirect evi-dence of prokaryotic organisms in some of the oldest sediments

organ-on earth, suggesting that life first appeared in the seas as soorgan-on

as the planet cooled enough for life as we know it today to ist There are three popular theories regarding the origin oflife on earth The classic theory, which dates from the 1950s,suggests that self-replicating organic molecules first appeared

ex-in the atmosphere and were deposited ex-in the seas by raex-in Inthe seas, these molecules underwent further reactions in thepresence of energy from lightning strikes to make nucleicacids, proteins, and the other building blocks of life More re-cently, the second theory has proposed that the first synthesis

of organic molecules took place near deep-sea hydrothermalvents that had the necessary heat energy and chemical activ-ity to form these molecules The third theory maintains thatorganic molecules came to Earth from another planet.The data suggest that the first eukaryotic cells appearedseveral billion years ago, but we know very few details aboutthe early evolution of these eukaryotes Although they ap-peared early, they probably took a few hundred million moreyears to develop into multicellular organisms Eukaryotic cellsare appreciably larger than prokaryotic cells and have a muchhigher degree of organization Each cell has a membrane-bound nucleus with chromosomes, and a cytoplasm contain-ing various specialized organelles that carry out differentfunctions, including reproduction An example of an organelle

is the mitochondrion Mitochondria serve as the sites of cellrespiration and energy generation The presence of these or-ganelles, and their similarity to the structures and functions

of free-living bacteria, suggest that bacteria were incorporatedinto the precursors of eukaryotic cells and lost their auton-omy in the process This scenario is referred to as the theory

of endosymbiosis; in essence, it defines the eukaryotic cell as

a community of microorganisms The first endosymbionts arebelieved to have been ancestral bacteria incorporating otherbacteria that could respire aerobically These bacteria subse-quently became the mitochondria The accumulation of freeoxygen in the oceans from photosynthesis may have triggeredthe evolution of eukaryotes; this hypothesis is supported bythe coincidental timing of the first eukaryotic cells and a rise

in the levels of free oxygen in the oceans On the basis of

fos-sil findings, scientists think that the forming of these early

complex cells took place rather quickly, probably between

2800 and 2100 million years ago (mya), even though the

old-est known eukaryote (Grypania, a coiled unbranched filament

up to 1.18 in [30 mm] long) comes from rocks that are more

than 2100 million years old The earliest eukaryotic cells

known to belong to any modern taxon are red algae, thought

to be about 1000 million years old

Data from the molecular clock suggest that the last

com-mon ancestor of plants and animals existed about 1.6 billion

years ago, which is long after the first appearance of

eukary-otes and long before any definite fossil records of metazoans

The Ediacaran fauna (600–570 mya) contains the first

evi-dence of the existence of many modern phyla This evievi-dence,

however, is largely a matter of trace fossils, which result fromanimals moving through sediment The relation of these tracefossils to modern phyla is therefore a matter of debate As of

2003, biologists tend to regard the entire fauna as includingmany species now viewed as primitive members of extantphyla The modern phyla thought to be represented amongthe Ediacaran fauna include annelid-like forms, Porifera,Cnidaria, Echiura, Onychophora, and Mollusca There aremany fossils from this period that cannot be assigned withcertainty to any recent phyla; these forms probably representhigh-level taxa that later became extinct Although most ofthe Ediacaran organisms were preserved as shallow-water im-pressions in sandstone, there are around 30 sites worldwiderepresenting deepwater and continental slope communities

CtenophoraCnidariaPlacozoa

XenoturbellidaChordataHemichordataEchinodermataBryozoaChaetognathaCephaloryncha

Micrognathozoa

NemerteaSipunculaPlatyhelminthes

MolluscaAnnelida

OnychophoraTardigradaArthropoda

Gnathostomulida

Entoprocta

CycliophoraRotifera

Gastrotricha

NematodaNematomorpha

Porifera

AcoelaMyzostomidaOrthonectidaDicyemidaNemertodermatida

PhoronidaBrachiopodaMetazoan phylogeny

The Ediacaran fauna was almost entirely soft-bodied,

al-though it also included some animals that palaeontologists

place among the mollusks and early arthropod-like organisms

They draw this conclusion from the fossilized remains of

chitinous structures thought to be the jaws of annelid-like

an-imals and the radulae (rows of teeth functioning as scrapers)

of mollusks Many of the animals from this period appear to

have lacked complex internal structures, but by the late

Edi-acara period larger animals appeared that probably had

in-ternal organs, considering their size For example, the

segmented sheet-like Dickinsonia, which was probably a

poly-chaete, grew as long as 39.3 in (1 m) It is unlikely that an

an-imal of that size could survive without internal structures that

digested and metabolized food It is clear from these fossils

that large and complicated metazoan animals already existed

540 mya

The amount of fossil evidence for bilaterally symmetrical

metazoans increased exponentially during the transition

be-tween the Precambrian and Cambrian Periods, about 544mya This transition is called the Cambrian explosion Thequestion is whether this sudden appearance of a number ofphyla is evidence for a rapid radiation (diversification) of an-imal forms Some researchers have suggested that the absence

or lack of metazoan life in the early fossils is due to the ple fact that the first animals were small organisms lackingstructures (like shells) that fossilized well Some findings sup-port the view that the first animals were microscopic; how-ever, as has already been mentioned, there were also largeanimals in this period Although there are problems with us-ing the molecular clock method of measurement (calibratingthe nodes in a phylogenetic tree based on assumptions aboutthe rate of mutations in a molecule), metazoan phylogeniesbased on molecular data indicate that many recent phyla ex-isted before the Cambrian explosion but did not leave fossilevidence until later Some researchers have proposed that amore complicated life style, more complex interactions amonganimals, and especially the advent of predation were a strong

sim-An illustration depicting what the ocean may have looked like during the Jurassic Period; present are an ammonite (Titanites anguiformis), based

on fossils from Portland, Dorset, England, and ichthyosaurs (Stenopterygius sp.), based on fossils from Holtzmanaden, Germany (Photo by Chase Studios, Inc./Photo Researchers, Inc Reproduced by permission.)

selective force for developing such features as shells as

an-tipredation devices While the Ediacaran fauna seems to have

consisted of suspension and detritus feeders who were largely

passive as well as a very few active predators, animal

com-munities during the Early Cambrian Period included most of

the trophic levels found in modern marine communities

Ac-cording to some authors, it is this second set of interactions

that led to structures that could be fossilized There have also

been explanations based on such abiotic factors as atmospheric

or geochemical changes In either case, it is possible that

al-though abundant fossils from the major animal phyla are

found in Cambrian strata, the organisms originated in an

ear-lier period In other words, the so-called “Cambrian

explo-sion” may simply reflect the difficulty of preserving

soft-bodied or microscopic animals Many paleontologists

hold that these phyla originated instead during the

Neopro-terozoic Period during the 160 million years preceding the

Cambrian explosion Their opinion is based on findings from

Ediacaran fauna

Dating the origins of the metazoan phyla is thus

contro-versial The resolution of this controversy has been sought in

DNA sequence data and the concept of a molecular clock

The molecular clock hypothesis assumes that the

evolution-ary rates for a particular gene are constant through time and

across taxa, or that we can compensate for disparate rates at

different times The results from such studies differ; however,

one relatively recent result indicates that protostomes and

deuterostomes diverged around 544–700 mya, and that the

divergence between echinoderms and chordates took place

just before the Cambrian period This study shows that

mol-lusks, annelids, and arthropods had existed for over 100

mil-lion years before the Cambrian explosion, and echinoderms

and early chordates may have arisen 50 million years prior to

this explosion

Protists

Although the term “protozoa” has been used for a long

time, and ranked as a phylum for a hundred years, it is now

clear that the name does not define a monophyletic group

“Protozoa” is really a name attached to a loose assemblage of

primarily single-celled heterotrophic eukaryotic organisms

The Kingdom Protista contains both organisms traditionally

called protozoa as well as some autotrophic groups (The

dis-tinction between heterotrophy and autotrophy is, however,

blurred in these organisms.) There are no unique features, or

synapomorphies, that distinguish this kingdom from others;

protists can be defined only as a grouping of eukaryotes that

lack the organization of cells into tissues and organs that is

seen in animals (or in fungi and plants for that matter)

Cur-rent understandings of protist phylogeny and classification are

in a state of constant flux Recent molecular studies have

over-turned so many established classification schemes that any

at-tempt to describe taxa within this kingdom as of 2003 risks

becoming obsolete in a matter of months In any event,

how-ever, the protists are the first eukaryotic organisms, and the

forerunners of the multicellular animals known as metazoans

One example of protists is phylum Ciliophora, the ciliates,

which are very common in benthic (sea bottom) and

plank-tonic communities in marine, brackish, and freshwater tats as well as in damp soils Several ciliates are important mu-tualistic endosymbionts of such ruminants as goats and sheep,

habi-in whose digestive tracts they convert plant material habi-into aform that can be absorbed by the animal Other examples in-clude the euglenids and their kin They are now placed in thephylum Kinetoplastida, but used to be part of what was calledthe phylum Sarcomastigophora, which, at that time, also con-tained the dinoflagellates (now placed in their own phylum Di-noflagellata) The phylum Kinetoplastida includes two majorsubgroups The trypanosomes are the better known of the two,since several species in this group cause debilitating and often

fatal diseases in humans Species of Leishmania cause a variety

of ailments collectively known as leishmaniasis, transmitted bythe bite of sand flies Leishmaniasis kills about a thousand peo-ple each year and infects over a million worldwide More se-

rious diseases are caused by members of the genus Trypanosoma

which live as parasites in all classes of vertebrates Chagas’

dis-ease, for example, is caused by a Trypanosoma species

trans-mitted to humans by a group of hemipterans (insects withsucking mouth parts) known as assassin or kissing bugs Theseinsects feed on blood and often bite sleeping humans (com-monly around the mouth, whence the nickname) They leavebehind fecal matter that contains the infective stages of thetrypanosome, which invades the body through mucous mem-branes or the insect’s bite wound

Other protists that cause serious diseases in humans

be-long to the phylum Apicomplexa Members of the genus

Plas-modium cause malaria, which affects millions of people in over

a hundred countries Malaria has been known since antiquity;the relationship between the disease and swampy land led to

the belief that it was contracted by breathing “bad air” (mal

aria in Italian) Nearly 500 million people around the world

Dorsal reconstruction of a crustacean (Waptia fieldensis) from the Middle Cambrian Burgess Shale of British Columbia This small, fairly common, shrimp-like arthropod had gill branches for swimming, tail flaps for steering, and legs for walking on the seafloor It averaged about 3 in (7.5 cm) in length (Photo by Chase Studios, Inc./Photo Researchers, Inc Reproduced by permission.)

are stricken annually with malaria; of these, 1–3 million die

from the disease, half of them children The most deadly

species of this genus, Plasmodium falciparum, causes massive

destruction of red blood cells, which results in high levels of

free hemoglobin and various breakdown products circulating

in the patient’s blood and urine These broken-down cellular

fragments lead to a darkening of the urine and a condition

known as blackwater fever

There are around 4000 described species of dinoflagellates,

now assigned to their own phylum, Dinoflagellata Many of

these species are known only as fossils There are fossils that

unquestionably belong to this group dating back 240 million

years; in addition, evidence from Early Cambrian rocks

indi-cates that they were abundant as early as 540 mya Some

planktonic dinoflagellates occasionally undergo periodic

bursts of population growth responsible for a phenomenon

known as red tide During a red tide, the density of these

di-noflagellates may be as high as 10–100 million cells per 1.05

quarts (1 liter) of seawater Many of the organisms that cause

red tides produce toxic substances that can be transmitted to

humans through shellfish Another well-known group of

pro-tists are the amoebas (phylum Rhizopoda), a small phylum of

around 200 described species The most obvious feature of

rhizopodans is that they form temporary extensions of their

cytoplasm known as pseudopodia, which are used in feeding

and locomotion

Earliest metazoans

The origin of the metazoan phyla is a matter of debate;

several theories are presently proposed The syncytial theory

suggests that the metazoan ancestor was a multinucleate,

bi-laterally symmetrical, ciliated protist that began to live on seabottoms A syncytium is a mass of cytoplasm that containsseveral or many nuclei but is not divided into separate cells.The principal argument in support of the syncytial theory isthe presence of certain similarities between modern ciliatesand acoel flatworms Most of the objections to this hypothe-sis concern developmental matters and differences in generallevels of complexity among the adult animals Another pro-posal known as the colonial theory suggests that a colonialflagellated protist gave rise to a planuloid (free-swimminglarva) metazoan ancestor The ancestral protist, according tothis theory, was a hollow sphere of flagellated cells that de-veloped some degree of anterior-posterior orientation related

to its patterns of motion, and also had cells that were cialized for separate somatic and reproductive functions Thistheory has been modified over the years by various authors;most evidence as of 2003 points to the protist phylumChoanoflagellata as the most likely ancestor of the Metazoa.Choanoflagellates possess collar cells that are basically iden-tical to those found in sponges There are a number ofchoanoflagellate genera commonly cited as typifying a po-

spe-tential metazoan precursor, for example Proterospongia and

Sphaeroeca.

The differences between the two theories may be rized as follows There is a ciliate ancestor in the syncytialtheory; this ancestor gave rise to one lineage leading to “otherprotists” and the Porifera (sponges), and another lineage lead-ing to flatworms, cnidarians, ctenophorans, flatworms, and

summa-“higher metazoans.” The colonial theory posits three rate lineages: one leading to other protists, a second toPorifera, and a third to the rest of the metazoans Both the-ories place Porifera at the base of the phylogenetic tree, prob-ably because sponges are among the simplest of livingmulticellular organisms They are sedentary filter feeders withflagellated cells that pump water through their canal system.Sponges are aggregates, or collections, of partially differenti-ated cells that show some rudimentary interdependence andare loosely arranged in layers These organisms essentiallyremain at a cellular grade of organization Porifera is the onlyphylum representing the parazoan type of body structure,which means that the sponges are metazoans without true em-bryological germ layering Not only are true tissues absent insponges, most of their body cells are capable of changing formand function

sepa-Diploblastic metazoans

The next step in the direction of more complex metazoanswas the evolution of the diploblastic phyla, the cnidarians andthe comb jellies “Diploblastic” refers to the presence of twogerm layers in the embryonic forms of these animals BothCnidaria and Ctenophora are characterized by primary radialsymmetry and two body layers, the ectoderm and the endo-derm One should note that some authors argue for the pres-ence of a third germ layer in the ctenophores that isembryologically equivalent with the other two PhylumCnidaria includes jellyfish, sea anemones and corals, togetherwith other less known groups Cnidarians lack cephalization,which means that they do not reflect the evolutionary ten-dency to locate important body organs in or near the head

A trilobite fossil (Ceraurus pleurexanthemus) from the Ordovician

Pe-riod, found in Quebec, Canada (Photo by Mark A Schneider/Photo

Researchers, Inc Reproduced by permission.)

In addition, cnidarians do not have a centralized nervous

sys-tem or discrete (separate) respiratory, circulatory, and

excre-tory organs The primitive nature of the cnidarian bauplan is

shown by the fact that they have very few different types of

cells, in fact fewer than a single organ in most other

meta-zoans The essence of the cnidarian bauplan is radial

sym-metry, a pattern that resembles the spokes of a wheel, and

places limits on the possible modes of life for a cnidarian

Cnidarians may be sessile, sedentary, or pelagic, but they do

not move in a clear direction in the manner of bilateral

cephal-ized creatures The cnidarians, however, have one of the

longest metazoan fossil histories The first documented

cnidarian fossil is from the Ediacaran fauna, which contains

several kinds of medusae and sea pens that lived nearly 600

mya There are two major competing theories about the

an-cestral cnidaria, focusing on whether the first cnidarian was

polyploid or medusoid in form According to one theory,

modern Hydrozoa lie at the base of the cnidarian phylogeny

(planuloid theory); other theories are inconclusive as to

whether the modern Anthozoa or Hydrozoa were the first

cnidarians

Ctenophores, commonly called comb jellies, sea

goose-berries, or sea walnuts, are transparent gelatinous animals

Like the cnidarians, the ctenophores are radially symmetrical

diploblastic animals that resemble cnidarians in many

re-spects They differ significantly from cnidarians, however, in

having a more organized digestive system, mesenchymal

mus-culature, and eight rows of ciliary plates at some stage in their

life history, as well as in some other features Although the

ctenophores and cnidarians are similar in their general

con-struction, it is difficult to derive ctenophores from any

exist-ing cnidarian group; consequently, the phylogenetic position

of ctenophores is an open question Traditional accounts of

ctenophores describe them as close to cnidarians but

separat-ing from them at a later point in evolutionary history

Ctenophores, however, are really quite different from

cnidar-ians in many fundamental ways; many of the apparent

simi-larities between the two groups may well reflect convergent

adaptations to similar lifestyles rather than a phylogenetic

re-lationship Ctenophores have a pair of anal pores that have

sometimes been interpreted as homologous with the anus of

bilaterian animals (worms, humans, snails, fish, etc.)

Fur-thermore, a third tissue layer between the endoderm and

ec-toderm may be a characteristic reminiscent of the Bilateria

These findings would support the phylogenetic position of

ctenophores in comparison to that of the cnidarians, but

re-cent molecular studies in fact point to a plesiomorphic

posi-tion “Plesiomorphic” refers to primitive or generalized

characteristics that arose at an early stage in the evolution of

a taxon As a result of these studies, the relationship between

cnidarians and ctenophores is still unsettled and is an active

area of research

Bilateral symmetry, triploblastic metazoans

and the protostomes

Although there are currently several different views

re-garding the details of metazoan phylogeny, all analyses make

a clear differentiation between the lower and diploblastic

an-imals on the one hand and the triploblastic anan-imals on theother Some time after the radiate phyla evolved, animals withbilateral symmetry (a body axis with a clear front end and backend) and a third germ layer (the mesoderm) appeared Theappearance of bilateral symmetry was associated with the be-ginning of cephalization as the nervous system was concen-trated in the head, and was accompanied by the development

of longitudinal nerve cords There are two fundamentally ferent patterns of mesoderm development, which are mir-rored in the two major lineages of the Bilateria, theDeuterostomia and the Protostomia This section will discussthe evolution of the protostomes It must be emphasized,however, that metazoan phylogeny is undergoing continualrevision The molecular data are inconclusive not only re-garding the relationships of some metazoan taxa to one an-other, but also which phyla belong to the two major clades.The following discussion of protostome evolution is derivedfrom the most recent analyses based on combinations of DNAand morphological data

dif-Most authors assign about 20 phyla to the Protostomia;however, recent molecular data and cladistic analyses based

on extended sets of morphological data do not agree as towhether the brachiopods and Phoronida should be includedamong the deuterostomes These analyses are also incongru-ent when it comes to the position of several phyla; in addi-tion, they call into question the monophyly of traditionallywell-recognized taxa Still, most authors have so far identifiedthe flatworms (Platyhelminthes) as the first phylum to emergeamong the protostomes Platyhelminths are simple, worm-like animals lacking any apomorphies that distinguish themfrom the hypothetical protostome ancestor An apomorphy is

a new evolutionary trait that is unique to a species and all itsdescendants The absence of apomorphies among the platy-helminths, then, means that there is no unique feature, such

as the rhyncocoel found in ribbon worms, that can be used

to identify the group as monophyletic Various hypotheses garding the origin of flatworms, their relationship to othertaxa, and evolutionary patterns within the group have beenhotly debated over the years Recent DNA data even suggeststhat the phylum Platyhelminthes is not monophyletic and thatone of the orders (Acoela) should be placed in a separate phy-lum These analyses furthermore place the flatworms in amore apomorphic position on the tree, indicating that whatwere regarded as primitive and ancestral conditions are reallyeither secondary losses, or that the ancestor was quite differ-ent from present notions of it

re-Morphological characters still suggest that the first tostomes were vermiform (worm-shaped) animals like the rib-bon worms in phylum Nemertea Other taxa with wormlikeancestral features include the sipunculans (phylum Sipuncula)and the echiurans (phylum Echiura), which are animals thatburrow into sediments on the ocean floor by using the largetrunk coelom for peristalsis The other major protostome taxaescaped from infaunal life, perhaps in part through the evo-lution of exoskeletons or the ability to build a tube The emer-gence of the mollusks may be an instance of this transition.The most primitive mollusks are probably the vermiformaplacophorans, or worm mollusks It seems likely that theseanimals arose from an early wormlike protostome, indicating

pro-that the sipunculans are related to the mollusks This

hy-pothesis is also supported by morphological data and 18S

rDNA sequences Except for the aplacophorans, all other

mol-lusks have solid calcareous shells produced by glands in their

mantles These shells, which provide structural support and

serve as defense mechanisms, vary greatly in size and shape

The most diverse group of animals with exoskeletons is

phylum Arthropoda, which includes over one million

de-scribed species, most of them in the two classes Crustacea

and Insecta The first arthropods probably arose in

Precam-brian seas over 600 mya, and the true crustaceans were

al-ready well established by the early Cambrian period The

arthropods have undergone a tremendous evolutionary

radi-ation and are now found in virtually all environments on the

planet The arthropods constitute 85% of all described

ani-mal species; this figure, however, is a gross underestimate of

the actual number of arthropod species Estimates of the true

number range from 3–100 million species The arthropods

resemble the annelids in being segmented animals; in

con-trast to the annelids, however, they have hard exoskeletons

This feature provides several evolutionary advantages but

clearly poses some problems as well Being encased in an

ex-oskeleton of this kind puts obvious limits on an organism’s

growth and locomotion The fundamental problem of

move-ment was solved by the evolution of joints in the body and

appendages, and sets of highly regionalized muscles The

in-tricate problem of growth within a constraining exoskeleton

was solved through the complex process of ecdysis, a specific

hormone-mediated form of molting In this process, the

ex-oskeleton is periodically shed to allow for increases in body

size It may be that ecdysis is unique to Arthropoda,

Tardigrada and Onychophora and not homologous to the

cu-ticular shedding that occurs in several metazoan phyla This

question is unresolved as of 2003 In the phylogeny included

here, the arthropods are assigned to the same clade (a group

of organisms sharing a specific common ancestor) as other

cuticular-shedding taxa Some authors refer to this clade as

Ecdysozoa, a classification that is receiving increasing port from various sources of information

sup-The development of an exoskeleton clearly conferred agreat selective advantage, as evidenced by the spectacularsuccess of arthropods with regard to both diversity andabundance This success took place despite the need for sev-eral coincidental changes to overcome the limitations of theexoskeleton One of the key advantages of an exoskeleton isprotection—against predation and physical injury, to besure, but also against physiological stress The morpholog-ical diversity among arthropods has resulted largely fromthe differential specialization of various segments, regions,and appendages in their bodies It is clear that segmenta-tion, in which body structures with the same genetic anddevelopmental origins arise repeatedly during the ontogeny

of an organism, is advantageous in general and leads to lutionary plasticity The segmented worms of phylum An-nelida exemplify this evolutionary plasticity This taxoncomprises around 16,500 species; annelids have successfullyinvaded virtually all habitats that have sufficient water An-nelids are found most commonly in the sea, but are alsoabundant in fresh water In addition, many annelid specieslive comfortably in damp terrestrial environments

evo-Segmentation as expressed in the arthropods and annelidshas traditionally been considered a character that indicates aclose relationships between these two taxa, and they are of-ten placed in the same clade Several recent analyses disputethis picture, however; the phylogeny included here assignsAnnelida and Arthropoda to two different clades It also placesthe flatworms in a much more apomorphic position and not

in their customary location at the base of the phylogenetictree Systematics and classification are unsettled as of 2003,and several “truths” about evolutionary relationships are likely

to be overturned in the near future These new phylogenieswill also lead to the revision of theories regarding the evolu-tion of behavior and characters

Resources

Books

Brusca, Richard C., and Gary J Brusca Invertebrates, 2nd ed.

Sunderland, MA: Sinauer Associates, 2003

Clarkson, Euan N K Invertebrate Palaeontology and Evolution,

4th ed Malden, MA: Blackwell Science, Ltd., 1999

Felsenstein, Joseph Inferring Phylogenies Sunderland, MA:

Sinauer Associates, 2003

Futuyama, Douglas J Evolutionary Biology, 2nd ed Sunderland,

MA: Sinauer Associates, 1998

Nielsen, Claus Animal Evolution, Interrelationships of the Living

Phyla Oxford, U.K.: Oxford University Press, 1995.

Periodicals

Giribet, Gonzalo, et al “Triplobastic Relationships withEmphasis on the Acoelomates and the Position ofGnathostomulida, Cycliophora, Plathelminthes, andChaetognatha: A Combined Approach of 18S rDNA

Sequences and Morphology.” Systematic Biology 49 (2000):

539–562

Nielsen, Claus, et al “Cladistic Analyses of the Animal

Kingdom.” Biological Journal of the Linnaean Society 57

Ontogeny and phylogeny

All animals must reproduce, passing copies of their genes

into separate new bodies in future generations These genetic

copies may be genetically identical, produced by asexual

processes, or genetically distinct, produced by sexual processes

In sexual processes, which are by far the more common among

animals, the initial result of reproduction is a single cell, known

as a zygote, containing the new and unique set of genes Yet,

by definition animals are multicellular, and generally consist

of hundreds, thousands, or millions of cells Even more

im-portant is the fact that the assemblage of cells that we

recog-nize as a given animal species must be orgarecog-nized into a specific

pattern This pattern, when viewed as a whole, defines the

morphology of the animal The morphology, in turn,

under-lies a complex functional organization of the animal in which

the cells are grouped into tissues (such as epidermis), organs

(such as kidneys), and organ systems (such as digestive

sys-tems) Each separate group of cells within an animal’s body

performs a specific function in what is called the division of

labor among body cells The processes through which the

sin-gle zygote becomes the complex multicellular adult animal,

with many tissues, organs, and systems in their proper places,

all functioning in a coordinated manner, are referred to as the

animal’s ontogeny

Clearly, the ontogeny of an animal is critical to

determin-ing what kind of creature the animal is and what it can

be-come Thus, it should be no surprise that specific ontogenetic

patterns tend to be characteristic of particular groups of

ani-mals For example, the leg of a crab and the leg of a mouse

are very different structures; the crab has an epidermal

ex-oskeleton around muscles, whereas the mouse has muscles and

epidermis around an internal bony skeleton The crab’s

struc-tural characteristics define it as a member of the phylum

Arthropoda; the mouse’s structural characteristics define it as

a member of the phylum Chordata Since structure must come

about through ontogeny, it stands to reason that each

mor-phologically distinct phylum of animals must also have a

dis-tinctive ontogenetic pattern So, taking it one step further, we

can reason that an animal’s ontogeny (the developmental

his-tory of the individual), correlates with its phylogeny (the

evo-lutionary history of the phylum)

Some nineteenth-century naturalists and biologists were

so struck by this relationship that they argued that an

ani-mal’s entire evolutionary history was repeated during thecourse of its embryonic development as an individual Laterstudies have shown that this exact repetition does not occur.However, the pattern of ontogeny is so important to an ani-mal’s formation that a basic correlation between ontogeny andphylogeny does exist For this reason, comparative zoologistshave long regarded patterns of embryonic development as be-ing crucial to the understanding of where each group of an-imals fits into the larger phylogenetic scheme

Protostomes vs deuterostomes

Given the long-standing recognition that embryonic velopmental patterns reflect evolutionary relationships, itcomes as no surprise that the two major branches of the an-imal kingdom are defined by differences in specific embry-onic attributes Early metazoans, such as sponges (phylumPorifera) and jellyfishes (phylum Cnidaria), have rather sim-ple bodies that exhibit a rather high degree of developmen-tal plasticity However, with the advent of flatworms (phylumPlatyhelminthes), we see greater complexity, and generallyless plasticity In flatworms and all higher animals, the bodyforms early into a three-layered embryo, and thus is said to

de-be triploblastic Each of the three layers is known as a germlayer, because it will form into all the organs of that bodylayer The outer ectoderm layer will develop into externalstructures such as the epidermis, skin, exoskeleton, nervoussystem, and sensory structures The middle mesoderm layerbecomes internal organs such as kidneys, reproductive sys-tems, circulatory systems, and muscles The inner endodermlayer will develop into the gut cavity and its derivatives, such

as the stomach, intestine, and liver

Above the level of flatworms, all higher animals possess anadditional mesodermal feature—a membrane-lined body cav-ity, or coelom This feature is so important that these higheranimals, which constitute more than 85% of animal species,are known collectively as coelomates But the coelom forms

in two very different ways, each of which corresponds ally with two very different sequences of basic embryonicevents Thus, the higher animals fall into two great branches,the Deuterostomia and the Protostomia, each defined by aunique set of embryonic characteristics The variations relate

gener-to (1) the pattern of cleavage; (2) the fate of the embryonic

• • • • •

Reproduction, development, and life history

blastopore formed during gastrulation; and (3) the method of

coelom formation The relevant characteristics among the

protostomes are described in the following sections

Gametogenesis

As higher animals, all sexually reproducing protostomes

form gametes, generally in the form of sperm (in male

sys-tems) and oocytes (in female syssys-tems) (Oocytes are sometimes

ambiguously called “eggs.”) Most protostomes are

gonocho-ristic, meaning that they have separate male and female

indi-viduals However, hermaphroditism, or the formation of male

and female gametes in the same individual, is very common

in many protostome phyla, reaching high levels in groups such

as the leeches and earthworms (phylum Annelida), and the

pulmonate snails (phylum Mollusca) Among hermaphrodites,sperm and oocytes can be produced by the same gonad, or byseparate male and female gonads, depending on the species

In any case, the basic processes of gamete formation, or metogenesis, are fundamentally similar in all phyla In allcases, it begins with reduction of the chromosome numberfrom paired sets to single sets, so that subsequent joining ofpairs from the male and female results in restoration of pairedsets After the reductional division, each gamete must take onstructural and functional characteristics that enable it to en-gage in pairing with the gamete of the opposite sex

ga-Spermatogenesis, the formation of sperm, thus begins withreductional division, then proceeds to development of a gen-erally motile and diminutive cell, capable of positioning itself

in physical contact with the oocyte Although it is technically

true that most sperm can swim, in some species sperm can

crawl, slither, or glide In each of these cases, however, it is

important to note that sperm cannot travel great distances;

the various propulsion devices, therefore, are more important

for small-scale positioning than for actually seeking out the

oocyte This is especially true of the many marine

proto-stomes that spawn their naked gametes directly into the

sea-water The formation of an individual sperm generally

involves extreme condensation of the chromosomes, and

elab-oration of motility devices such as flagella, oocyte-encounter

and oocyte-manipulation devices, and energy stores

An important aspect of spermatogenesis in most species is

the close synchronization of sperm development and release

The primary basis for synchronization is the maintenance of

close physical contact between the spermatogenic cells

throughout their development In virtually all cases, this

con-tact involves the actual sharing of a common cell membrane

and cytoplasm among large clusters of cells These clusters

are known as spermatogenic morulae In annelid worms,

vel-vet worms (phylum Onychophora), and some other

proto-stome groups, these morulae have the appearance of balls of

sperm, all within a large saclike gonad or the body cavity, with

the heads pointed inward and the tails pointing outward In

shrimp, lobsters, and other crustaceans, as well as insects

(phy-lum Arthropoda), the morulae occupy individual chambers in

the gonad In snails, clams, and their relatives (phylum

Mol-lusca), the morulae often occur in concentric rings, with the

less-developed cells in the outer rings, near the gonad wall,

and the more-developed cells in the central rings, near to the

ducts leading to the outside

Oogenesis, the formation of oocytes, also begins with a

re-ductional division of the chromosomes, but then proceeds to

the formation of a generally large, spherical, nonmotile cell

The oocyte does not generally contribute to preliminary

po-sitioning with the sperm, but it does play a vital role in

bring-ing the two gametes to a point of fusbring-ing to form a sbring-ingle

composite cell, the fertilized zygote In fact, contrary to

pop-ular belief, it is more correct to say that the oocyte fertilizes

the sperm, rather than that the sperm fertilizes the oocyte In

reality, both gametes make vital contributions to this union,

but it is clearly the oocyte that is responsible for most of what

happens after that During oogenesis, the oocyte is equipped

with special structures and regulatory enzymes for

internal-izing the sperm nucleus, directing the fusion of the two

nu-clei, setting up the rapid sequence of cell divisions that follow,

and even establishing the patterns of division and subsequent

embryonic events Following fertilization, most protostomes

develop rapidly into a fully functional feeding larva or

juve-nile, and the oocyte must take care of all the needs of the

de-veloping embryo until it is capable of feeding on its own

Thus, in addition to the mechanical and regulatory

appara-tus, the oocyte generally must contain large nutrient stores in

the form of lipid- and protein-rich yolk

Some protostomes regularly engage in sexual

reproduc-tion, yet do not require the development of both sperm and

oocytes In many of these cases, the species are technically

gonochoristic, but males are rarely or never produced

How-ever, if the offspring develop from true oocytes, with the

re-duction of chromosome number, even without subsequentfertilization, this is a form of sexual reproduction If no trueoocytes are formed by the reductional division of the chro-mosomes, the reproduction is asexual, even though the prog-eny cells look like oocytes Whether sexual or asexual, thistype of reproduction by female-only species is known asparthenogenesis Among protostomes, some insects (phylumArthropoda) are well known for their parthenogenetic capa-bilities

Copulation, spawning, and fertilization

Because gametes are capable of limited or no motility ative to the vast habitat in which the animals live, each speciesmust have a way of bringing the sperm and oocytes close toeach other so that fertilization can occur The mechanismsfor doing this are numerous, and involve a dazzling diversity

rel-of behavioral and anatomical modifications across the trum of protostome life Despite the diversity, all can begrouped generally into two broad categories, copulation andspawning

spec-Copulation involves various mechanisms by which onemember of a mating pair physically introduces sperm into thebody of its partner In hermaphroditic species, this insemina-tion is usually reciprocal The precise mechanism of insemi-nation varies among protostome groups, as does the site ofinsemination Many snails (phylum Mollusca), especially ma-rine prosobranchs, possess a large penis that can extend allthe way out of the shell of the male and into the mantle cav-ity of the female, depositing sperm directly in the genitalopening Many male crustaceans and insects (phylum Arthro-poda) have complex exoskeletal structures, derived from spe-cific appendages or body plates, which lock mechanically withcomplementary plates surrounding the genital opening of thefemale Some protostomes transfer special packets of sperm,known as spermatophores, to their mating partner, so that theindividual sperm can be released into the female’s systemsome time after copulation has ended For example, malesquids (phylum Mollusca) use a modified arm to place a loadedspermatophore inside the mantle cavity of a female Some her-maphroditic leeches (phylum Annelida) actually spear theirmating partner through the skin with a dartlike sper-matophore, which slowly injects the sperm through the bodywall following copulation In almost all cases, whether bysperm or spermatophore transfer, copulation is followed byinternal fertilization, and at least some degree of internal de-velopment The benefits of internal fertilization and devel-opment are especially great in terrestrial environments, sovirtually all terrestrial protostomes copulate Likewise, thefreshwater environments are not generally hospitable for ga-metes and embryos, so most freshwater protostomes are cop-ulators, although there are some exceptions

The vast majority of marine invertebrates are broadcastspawners, meaning that they broadcast their gametes freelyinto the open seawater A few freshwater species, such as thewell-known invasive zebra mussel (phylum Mollusca) also en-gage in broadcast spawning In most cases of broadcast spawn-ing, both the sperm and oocytes are spawned so thatfertilization is external But in a few groups, such as some

clams and other bivalve mollusks, only the males spawn,

leav-ing the adult females to draw sperm into their bodies for

in-ternal fertilization Following inin-ternal fertilization, many

species brood their young for some period of time, either

in-ternally, as in some snails, or externally in egg masses, as in

some decapod crustaceans Even among broadcast spawners

with external fertilization, some species take up embryos or

larvae from the open water and brood them internally, or

brood them externally on the body surface

For most protostomes, sexual reproduction is highly

peri-odic, so copulatory and spawning behavior are also periodic

Focusing all gamete-releasing into defined periods of time is

yet another way that the fully formed gametes can achieve

higher rates of success in encountering one another Among

terrestrial and freshwater species, the periodicity is generallyannual, occurring only at certain seasons of the year Thesame may be true for marine species, particularly in near-shore environments, where seasonal runoff of rainwater fromrivers provides seasonal cues for sexual activity, as well as sea-sonal surges in nutrients to feed the resulting larvae In othermarine environments, reproductive periodicity is often influ-enced more by lunar or tidal rhythms, and so may occur inmonthly rather than in annual cycles

cuticle Ear thworm Hydrostatic Skeleton

waxy layer rigid chitinous layer flexible chitinous layer

epidermis

periostracum prismatic layer pearly layer

as embryogenesis The actual establishment of

multicellu-larity from the unicellular zygote involves a process known

as cleavage Cleavage involves more than simple cell

divi-sion, for example, mitosis True multicellularity involves the

division of labor among cells, so each cell has to take on a

special identity and developmental fate shortly after

becom-ing independent of its progenitor cell The process of

ac-quiring a distinctive function is known as differentiation, and

acquiring a specific developmental fate is known as

deter-mination Protostomes generally undergo differentiation and

determination very early in development, in many cases at

the very first cell division of cleavage This is easily visible

under a standard microscope for some phyla, but is hidden

from view by the highly modified cleavage patterns of

in-sects, spiders, and some other arthropods

The first thing that distinguishes protostomes fromdeuterostomes is this early determination Thus, protostomesare often said to undergo determinate cleavage, or mosaic de-velopment, in contrast to the indeterminate cleavage, or reg-ulative development, of deuterostomes These two cleavagepatterns are so different that they can be distinguished easilywith a microscope The determinate cleavage of protostomesresults from a plane of cell division, usually visible after thesecond division, that cuts diagonally across the original zy-gote axis, thus compartmentalizing different regulative andnutritive chemicals in each of the resulting cells This is re-ferred to as spiral cleavage, since the cells dividing diagonallyappear under the microscope to spiral around the originalaxis In contrast, the indeterminate cleavage of deuterostomesresults from planes of cell division that cut alternatively lon-

coxa basis ischium merus carpus propodus dactylus siphon

Locomotion in different animals: A Squid propulsion; B A snail’s muscular foot; C Leg extension in arthropods (Illustration by Patricia Ferrer)

gitudinally along the zygote axis, then transversely across the

axis, thus leaving each resulting tier of cells with similar

reg-ulative and nutritive chemicals This is referred to as radial

cleavage, since the cells dividing at alternating parallel and

right angles to the original axis appear under the microscope

to radiate in parallel planes from that axis The most

impor-tant thing is not whether the resulting cell masses appear to

spiral or to radiate, but that the spiraling cells of the

proto-stomes show determination of specific germ layers as early as

the first cell division, and almost universally by the third

Thus, at the very earliest stages of cleavages, specific cells of

protostomes have already been determined to a fate of

form-ing one of the three germ layers

Within these basic functional forms of cleavage, there are

many variations in the specific spatial configurations and the

extent of cell division Most protostomes undergo some type

of holoblastic cleavage, in which the two daughter cells

be-come completely separated, each with its own complete cell

membrane This type of cleavage may be described as either

equal cleavage or unequal cleavage, depending on whether the

daughter cells are equal in size Most protostomes exhibit

un-equal holoblastic cleavage In all these, the large cells are

called macromeres, and they usually form the endoderm and

the mesoderm Small micromeres at the other end of the

em-bryo generally form the ectoderm Some animals have someres of an intermediate size, which may contribute to ei-ther the ectoderm or the mesoderm, depending on the species

me-In contrast, many arthropods with very large, heavily yolkedoocytes undergo a form of incomplete cleavage known as su-perficial cleavage, in which the incompletely divided daugh-ter cells ultimately reside as a layer surrounding a shared yolkmass This appears similar to the meroblastic cleavage seen

in large yolky eggs of birds and reptiles, but true superficialcleavage in arthropods begins with multiple divisions of thenuclei prior to the division of the cytoplasm

Blastulation, gastrulation, and coelom formation

During and after cleavage, embryonic development tinues with a series of rearrangements among the cells andcell layers In the first of these, known as blastulation, thecells in the solid mass resulting from cleavage simply arrangethemselves in preparation for the establishment of the spa-tially segregated germ layers Blastulation begins during themiddle-to-late stages of cleavage, and varies in the degree oflayer organization The final blastula stage of most proto-stomes is a solid mass of cells, known as a stereoblastula Typ-

con-When scorpion offspring are born, the mother assists them in climbing onto her back, where they stay until their first molt They then climb down, and live independently (Photo by A Captain/R Kulkarni/S Thakur Reproduced by permission.)

ical examples of this can be seen among many marine

mol-lusks and annelids In some protostomes, the blastula stage,

known as a coeloblastula, is a hollow ball of cells that are

arranged in a single layer around the central cavity, known

as a blastocoel The ribbon worms (phylum Nemertea) are

not considered coelomates by most biologists, and therefore

are not technically protostomes However, they undergo

typ-ical spiral cleavage and develop through a coeloblastula stage

and exhibit other protostome characteristics, so most

biolo-gists consider them to be closely related to the protostomes

After blastulation, the blastula is now ready to undergo a

critical process in which the three embryonic germ layers are

established This process is known as gastrulation, since it is

characterized by the internalization of the endodermal cells

to form the archenteron, which is the ancestral

gastrointesti-nal tract Gastrulation involves a specific set of cell

move-ments that vary widely, depending on the animal group These

mechanisms range from invagination, to inward migration, to

inward growth and proliferation The end result, however, is

the same The endodermal cells are now internal, forming the

archenteron gut tube, while the mesodermal cells take up

res-idence between the endoderm and the ectoderm, which

com-prises cells that remained on the outside of the embryo

Regardless of how the gastrulation process takes place, the

embryo is left with an opening to the outside; this opening,

the blastopore, is encircled by a rim that forms the boundary

between endoderm and ectoderm, and will develop into an

opening into the gut in the adult animal The precise nature

of the opening is the second major defining attribute of the

protostomes, in which the fate of the blastopore is to form

the adult mouth Conversely, the fate of the blastopore in

deuterostomes is to form the anus

Shortly or immediately after gastrulation is complete,

pro-tostomes form their body cavity, the coelom By definition, a

true coelom is always a body cavity within mesodermal

tis-sue The mechanism by which the coelom is formed is the

third primary distinction between protostomes and

deuteros-tomes In most deuterostomes, the coelom forms by

out-pocketing from the original archenteron, a process known as

enterocoely, since the coelomic cavities are thus derived

di-rectly from embryonic enteric cavities In protostomes, the

coelom forms from a split in the previously solid mass of

mesodermal cells, a process thus known as schizocoely There

are some exceptions to this rule, but it holds true in most

cases Some protostomes lack a coelom as adults, but even

these typically go through a coelomate embryonic and/or

lar-val stage

Larval and postlarval development

The gastrula stage is technically the last stage of

embry-onic development, so every stage following, up to the adult,

is postembryonic Many protostomes undergo postembryonic

development that is direct In these cases, the gastrula

devel-ops directly into a juvenile, which is typically a miniature, but

sexually immature, version of the adult The juvenile then has

simply to grow and mature to become an adult The vast

ma-jority of protostomes take a very different approach,

engag-ing in a more complex pattern known as indirect development

This involves the development of the gastrula into some sort

of distinctive larva, which is both immature and quite ent from the adult Typically, larvae have functions in the lifehistory that are critical to the species, yet differ from that ofthe adult In most marine protostomes, the primary function

differ-of the larval form is to provide for the dispersal differ-of the species

to colonize new habitats Larvae are generally well suited forthis since they are very small, and thus easily carried freelyfloating in the water as plankton This planktonic dispersal oflarvae is especially well developed among the marine annelids,mollusks, and crustaceans, but also occurs in the minor pro-tostome phyla, such as Echiura and Sipuncula

Larvae occur in many types, depending on the phylum andspecies, and each of these types has been given a specific name

In the simplest forms, such as with marine mollusks and nelids, the trochophore is little more than a gastrula withbands of cilia for swimming At the other end of the spectrum

an-of complexity, marine crustaceans may go through a sion of anatomically distinct larval stages, such as the nau-plius, zoea, or megalopa Larvae of all groups rely onconsiderable nutrients as they disperse and develop, but theyacquire them in different ways Depending on the species,they are either planktotrophic, feeding on plankton as theydrift, or lecithotrophic, relying on stored yolk material ob-tained from the mother Regardless of the number or type oflarval stages, each species will eventually undergo metamor-phosis, a dramatic change of morphology into the adult form

succes-In some species, there is an intermediate juvenile stage, sothat postembryonic development is mixed, having indirect anddirect components Insects are especially variable in this re-gard In the case of freshwater insects, the larval and juvenilestages are often the dominant stage in the life cycle In some

of these, such as caddisflies and mayflies, the larvae may livefor one to several years, whereas the adult lives for only days

In some terrestrial insects, such as cicadas, the larvae may live

up to 17 years, with the adults living only a few weeks Incases such as these, the larva actually defines the species eco-logically, and the adult is simply a short-lived stage necessaryfor sexual reproduction

Sexual maturation

The final stage of postembryonic development is sexualmaturation This is preceded by the final development of crit-ical body parts, and even of the fundamental body framework,

as in the segmentation, or metamerism, of annelids andarthropods Sexual maturation may occur immediately fol-lowing embryonic development, or may be arrested for manyyears Many protostomes undergo sequential cycles of sexualmaturation, growing gonads and/or gametes during certainseasons, and completely losing them in others During non-reproductive periods, such an animal may appear to be a largejuvenile Notable among these are the many marine poly-chaete worms (phylum Annelida) that lack distinct gonads,but whose gametes form from mesodermal peritoneal cellslining the coelom only when the proper environmental cuesinduce them to transform

The most important variation among postembryonic togenetic strategies involves the degree to which animals can