Phylum Granuloreticulosa:Foraminiferans and Their Kin 105
Phylum Radiolaria: Radiolarians 108
Phylum Haplosporidia: Haplosporidians 111
Group 4: Excavata 112
Phylum Parabasalida: Trichomonads, Hypermastigotes, andTheir Kin 112
Phylum Diplomonadida: Diplomonads 115
Phylum Heterolobosea: Heterolobosids 117
Phylum Euglenida: Euglenids 118
Phylum Kinetoplastida:Trypanosomes, Bodonids, andTheir Kin 120
Group5: Opisthokonta 124
Phylum Choanoflagellata: Choanoflagellates 124
CHAPTER 4
Protist Phylogeny 125
The Origin ofthe Protista 125
Relationshipsan1ongthe Protists 127
Introduction to the Animal Kingdom: Animal Architecture and Body Plans 135
Body Symmetry 136
Cellularity, Body Size, Germ Layers, and Body Cavities 138
Locomotion and Support 140
Feedingand Digestion 148
Excretion andOsmoregulation 157
Circulation andGas Exchange 162
NervousSystems andSenseOrgans 168
CHAPTER 5
Bioluminescence 174
Nervous Systems and BodyPlans 174
Hormones andPheromones 175
Reproduction 176
AsexualReproduction 176
SexualReproduction 177
Parthenogenesis 179
Introduction to the Animal Kingdom: Development, Life Histories, and Origin 183
EvolutionaryDevelopmental Biology-EvoDevo 184
DevelopmentalToolKits 184
The RelationshipBetv1eenGenotypeand Phenotype 185
TheEvolution ofNovelGene Function 185
Gene RegulatoryNetworks 185
Eggs and Embryos 187
Eggs 187
Cleavage 187
Orientation ofCleavage Planes 188
Radialand SpiralCleavage 188
CellFates 191
BlastulaTypes 192
Gastrulationand Germ Layer Formation 193
MesodermandBody Cavities 195
LifeCycles: Sequences and Strategies 197
Classificationof LifeCycles 197
IndirectDevelopment 197
Settling and Metamorphosis 199
DirectDevelopment 199
Mixed Development 200
Adaptations to LandandFresh\iVater 200
Parasite LifeCycles 200
CHAPTER 6
The Relationships BetweenOntogeny and Phylogeny 201
The Origin ofthe Metazoa 203
Two Basal Metazoan Phyla: Porifera and Placozoa 213
PhylumPlacozoa 215
PhylumPorifera:The Sponges 216
Taxonomic History and Classification 220
The Poriferan Body Plan 222
Some AdditionalAspects of Sponge Biology 249
CHAPTER 7
DistributionandEcology 249
Biochen1icalAgents 250
Growth Rates 250
Sy1nbioses 251
Poriferan Phylogeny 254
The Origin ofSponges 254
Evolution within thePorifera 255
Phylum Cnidaria: Anemones, Corals, Jellyfish, andTheir Kin 265
Taxonomic History and Classification 268
The Cnidarian Body Plan 274
Cnidarian Phylogeny 317
CHAPTER 8
EdiacaranCnidaria? 317
Cnidarian Origins 318
Relationships withinCnidaria 319
Phylum Ctenophora: The CombJellies 327
Taxonomic History and Classification 328
The Ctenophoran Body Plan 332
CHAPTER 9
CtenophoranPhylogeny 341
Introduction to the Bilateria and the Phylum Xenacoelomorpha: Triploblasty and Bilateral Symmetry Provide New Avenuesfor Animal Radiation 345
TheBasal Bilaterian 346
Protostomes andDeuterostomes 347
PhylumXenacoelomorpha 349
Classificationof PhylumXenacoelomorpha 35
Class Acoela 351
The Acoel Body Plan 353
Class Nemertodermatida 360
The Nemertodermatid Body Plan 362
Subphylum Xenoturbellida 366
The Xenoturbellid BodyPlan 367
CHAPTER 10
Phylum Platyhelminthes: The Flatworms 373
Taxonomic History andClassification 374
The Platyhelminth Body Plan 380
CHAPTER 11
Platyhelminth Phylogeny 405
Four Enigmatic Protostome Phyla: Rhombozoa, Orthonectida, Chaetognatha, Gastrotricha 413
Phylum Rhombozoa 414
The Dicyemida 414
TheHeterocyemida 417
Phylum Orthonectida 418
Phylum Chaetognatha 420
CHAPTER 12
Chaetognath Classification 422
TheChaetognath Body Plan 423
PhylumGastrotricha:The Gastrotrichs 428
Gastrotrich Classification 429
The Gastrotrich Body Plan 429
Phylum Nemertea: The Ribbon Worms 435
Taxonomic History andClassification 436
The Nemertean Body Plan 438
CHAPTER 13
Phylum Mollusca 453
Taxonomic History andClassification 454
The Molluscan Body Plan 472
CHAPTER 14
Phylum Annelida: The Segmented(andSome Unsegmented) Worms 531
Taxonomic History andClassification 532
The AnnelidBodyPlan 541
Sipuncula: The Peanut Worms 572
Sipunculan Classification 574
The Sipunculan Body Plan 575
Echiuridae:The SpoonWorms 579
Siboglinidae:VentWorms and TheirKin 584
SiboglinidTaxonomic History 588
The Siboglinidae Body Plan 588
Hirudinoidea: Leeches andTheir Relatives 591
The Hirudinoidean Body Plan 592
Annelid Phylogeny 597
Nemertean Phylogeny 450
Molluscan EvolutionandPhylogeny 521
CHAPTER 15
Two Enigmatic Spiralian Phyla: Entoprocta and Cycliophora 603
PhylumEntoprocta:The Entoprocts 603
Entoproct Classification 605
CHAPTER 16
The Entoproct BodyPlan 606
Phylum Cycliophora: TheCycliophorans 609
The Gnathifera: PhylaGnathostomulida, Rotifera(including Acanthocephala), and Micrognathozoa 613
PhylumGnathostomulida: The Gnathostomulids 615
Gnathostomulid Classification 615
The Gnathostomulid Body Plan 616
PhylumRotifera:TheFree-Living Rotifers 616
RotiferClassification 618
The RotiferBody Plan 618
Phylum Rotifera, Subclass Acanthocephala: The Acanthocephalans 624
The Acanthocephalan Body Plan 624
PhylumMicrognathozoa:The Micrognathozoans 626
CHAPTER 17
The Lophophorates: Phyla Phoronida, Bryozoa, and Brachiopoda 635
Taxonomic History of the Lophophorates 636
The Lophophorate Body Plan 637
PhylumPhoronida:ThePhoronids 638
ThePhoronid Body Plan 638
CHAPTER 18
Phylum Bryozoa: The Moss Animals 644
TheBryozoan Body Plan 646
Phylum Brachiopoda: The Lamp Shells 657
The BrachiopodBody Plan 660
The Nematoida: Phyla Nematoda and Nematomorpha 669
PhylumNematoda: Roundworms and Threadworms 671
Nematode Classification 672
TheNematode Body Plan 673
CHAPTER 19
Life Cycles of Some Parasitic Nematodes 682
Phylum Nematomorpha: HorsehairWorms and Their Kin 686
TheNematomorphan Body Plan 687
The Scalidophora: Phyla Kinorhyncha, Priapula, and Loricifera 693
PhylumKinorhyncha:The Kinorhynchs 695
Kinorhynch Classification 696
The Kinorhynch BodyPlan 696
Phylum Priapula: The Priapulans 698
Priapulan Classification 699
The Priapulan Body Plan 699
Phylum Loricifera: The Loriciferans 701
The Micrognathozoan Body Plan 628
CHAPTER 20
The Emergence oftheArthropods: Tardigrades, Onychophorans, and the Arthropod Body Plan 709
PhylumTardigrada 711
TheTardigradeBody Plan 715
Phylum Onychophora 718
The Onychophoran Body Plan 722
An Introduction to the Arthropods 728
TaxonornicHistoryandClassification 728
The Arthropod BodyPlan and Arthropodization 730
The Evolution ofArthropods 751
TheOriginofArthropods 751
Evolution1,vithin theArthropoda 751
CHAPTER 21
PhylumArthropoda: Crustacea: Crabs, Shrimps, andTheir Kin 761
Classification ofThe Crustacea 764
Synopses of Crustacean Taxa 767
CHAPTER 22
The CrustaceanBody Plan 798 Crustacean Phylogeny 831
PhylumArthropoda: The Hexapoda: Insects and Their Kin 843
HexapodClassification 847
The Hexapod Body Plan 859
CHAPTER 23
Hexapod Evolution 887
PhylumArthropoda: The Myriapods: Centipedes, Millipedes, and Their Kin 895
MyriapodClassification 897
The Myriapod Body Plan 899
CHAPTER 24
Myriapod Phylogeny 908
PhylumArthropoda: The Chelicerata 911
ChelicerateClassification 915
The Euchelicerate Body Plan 927
The Class Pycnogonida 955
ThePycnogonidBody Plan 958
Chelicerate Phylogeny 961
CHAPTER 25
Introduction to the Deuterostomes and the Phylum
Echinodermata 967
PhylumEchinodermata 968
Taxonomic History and Classification 969
The Echinoderm Body Plan 975
CHAPTER 26
Echinoderm Phylogeny 1000
First Echinoderms 1000 Modern Echinoderms 1001
Phylum Hemichordata: Acorn Worms and Pterobranchs 1007
Hemichordate Classification 1008
TheHemichordate Body Plan 1009
Enteropneusta (Acorn Worms) 1009
CHAPTER 27
Pterobranchs 1015
Hemichordate Fossil Record and Phylogeny 1018
Phylum Chordata: Cephalochordata and Urochordata 1021
ChordateClassification 1022
PhylumChordata,SubphylumCephalochordata:
The Lancelets (Amphioxus) 1023
TheCephalochordateBody Plan 1041
CHAPTER 28
Phylum Chordata, Subphylum Urochordata: The Tunicates 1027
The Tunicate Body Plan 1041
Chordate Phylogeny 1041
Perspectives on Invertebrate Phylogeny 1047
Illustration Credits 1053
Index 1061
Preface to the Third Edition
or this edition of Invertebrates, Wendy Moore and Stephen M.Shusterjoined as co-authors. In addition, 22 other contributingauthors graciously agreed to revise selected chapters or chapter sections. And two dozen reviewers were kind enough to critically read various chapters of the book. Thereislikelyno wayInvertebrates,Third Edition could have the depthand accuracy it haswithoutthe help of these wonderful professionals and specialists, and we are deeply indebted to them.
An information explosion has occurred since the Second Edition of this book, especially in the fields of molecular biology and phylogenetics. Just as the Second Edition of Invertebrates was going into production, the beginning framework of a new n1etazoan phylogeny was starting to appear in the scientific literature, although at that time it was based aln1ost entirely on ribosomal gene trees and considerable disagreementexisted. In theinterveningdecade, this new phylogeny,,vas refined althoughmany detailsstill remain to be worked out. Mostilnportantly, Protostomia and Deuterostomia have been redefined, and the long-standingArticulata group(based upon a hypothesized sister-group relationship between Annelida and thePanarthropoda) has been disarticulated with annelids now being placed among the Spiralia, and arthropods amongthe Ecdysozoa. The phyla Echiura and Sipuncula have been subsumed into Annelida. The basal, diploblasticphyla havebeenshuffled about near the baseof the Metazoa tree, and they might continue to shuffle about for a bit longer; as this edition goes to press. We predict iliat, by theFourth Edition of Inverte/1rates, the phylogeneticpositionsof all (or at least most) of thernetazoan phyla will be stabilized-a lofty goallong soughtby zoologists.
Asin theSecond Edition, important new terms are printed in boldface when first defined (and these are noted in the Index). Specific gene names, like species
names,areitalicized (though note thatnames for classesof genes,e.g., Hox and ParaHox genes, are not italicized).We have again included the protists inthe book, because instructors teachingInvertebrateZoology usually cover the "kingdom Protista" and have asked for it.Our knowledge of protistan biology andphylogeny has expanded so much since the Second Edition that the an1ount of new information, even briefly presented, is substantial. The ICZN (International Code for Zoological Nomenclature) eschews use of diacritical marksin formal taxonomic names, and ,,ve follow that recommendation.However, forotherterms we generally retain the originalspellings and diacritics. So for example,there arearchoophoran andneoophoranflatworms (the terms describing modes of egg development), but there arealso the (now largely abandoned) taxa Archoophoraand Neoophora.
Much of ilie art for this edition has been updated. However, "''e continue toinclude diagrams that will be useful to students in the laboratory, including for aniiual dissections. We also continue toprovide rather detailed classifications andtaxonomicsynopses within each phylum. Wedon'texpecttheseto read in the same way asthe restof the chapter,but rather to be used as a reference to lookuptaxonomicnames,understandthe traits that distinguishgroups,or getan overall senseof thescope of iliehigher taxa in a phylum.
To say this book is a "labor of love" would be an understatement.Without a deep passion for mvertebrates, onthepart of all the contributors, it would not havebeenpossible. Hope.fullythisbook elevates in its readerstheir own passion and enthusiasm for iliat96% of the animal kingdom that has so successfully flourished without backbones.
uring the revisionof Invertebrates my brother Gary passed away. For a while the project was stalled. But, buoyed by the support of family, friends, and colleagues, I eventually returned to the task, which, at times, seemed overwhelming. The field of invertebrate biology is so vast, and cuts across so n1any disciplinary lines, that even in a book of this size it is necessary to generalize about some topics and to slight others. As university instructors, my brother and Irealized early onthat the teaching of invertebrate zoology should not be compartmentalized. Thus, in planning this book we were concerned about two potentialdangers. First, the text might become an encyclopediclist of "facts" about one group after another, the sort of "flash-card" approach thatwe wanted to avoid. Second, the book might be a rambling series ofstoriesor vignettes about randomly selected animals (or "model organisms'') and their ways of life. The first book would be dull, would encourage rote memorization instead of understanding, and might give the misconception that there is little left todiscover. Thesecond bookmight befull of interesting "gee whiz" stuff but would seem disorganized and ,,vithout continuity or purpose to the serious student. Either approach could fail to present the most important aspectsofinvertebrates their phenomenal diversity, their natural history, and their evolutionary relationships. We also held to the belief that v.-hat we kno,v about these animals is not as important as how we think about them. You should be prepared to assimilate much new material, but you should also be prepared for a great deal of uncertainty and mystery, as much remainstobe discovered.
To avoid the pitfalls noted above, and to establish threads of continuity in our discussions about invertebrates, we developed our book around two fundamental themes: unity and diversity. The first theme we approach by way of functional body architecture,
or whatwe callthebauplanconcept.The second theme \Ve approach through the principles of phylogenetic biology. Our hope was thatweaving the book tightly to these themes would provide a 1neaningful flow as readers move fromone phylum to the next. The first fivechapters provide backgroundfor thesethemes and thus provide an importantfoundation upon which the restof the book rests. Please readthese chapters carefullyand refer back tothemthroughoutyourstudy.
The bulk of this bookis devoted to a phylum-byphylum discussion of invertebrates. Fairly detailed classificationsor taxonomic synopses for eachphylUJn are included in separate sections of each chapter to serveasreferences.A consistent organization ismaintainedthroughout each chapter, although �ve did yield tothe important and sometimesdifferent lessons to be learned by investigating the special attributes of each group of animals. Inaddition,becauseof their size and diversity, some taxa receive more attention than others although thisdoes not n,ean that such groups are more "i1nportant" biologically than smaller or more ho1nogeneous ones. (Five chapters are devoted to the arthropods and their kin.) In certain chapters more than one phylum is covered. In some cases the phyla coveredarethought to be closelyrelated toone another;in other cases the phyla merely represent a particular gradeof complexity and their inclusion in a single chapter facilitatesour comparative approach.
Certain aspects of this book have, of course, been influenced byourown biases; thisis especially true of the discussions onphylogeny. We use acombination of phylogenetic trees (cladograms) and narrative discussions to talk about animal evolution. Cladograms are used when appropriate, because theyprovidethe least ambiguous state1nents that can be made about animal relationships. We always knew that some of you, professors and students both, would disagree with our methods and ideas to various degrees at least we hopedthat youwould.Never placidly accept what you see in a textbook, or anyplace else for that matter, but try tobe critical in your reading.
Thebook's final chapter isa phylogenetic summary of the animal kingdon1.It reinforces the point that
much remains to beexplored and learned about the evolutionaryrelationsh.ipsofinvertebrates.Likeall scientificknowledge, wearedealing herewithprovisional,transient"truths"thatalwaysremainopentochallengeandrevision.And,of course,scientistsdisagree. Itisth.is disagreementandtheconstant challengingof hypothesesthatenliventhefieldandpushthefrontiers ofknowledgeforward.
Thereareafewotherthingsyoushouldknowabout this book.Abriefhistorical reviewof theclassification of each tnajorgroup isprovided.Wefelt thismaterial wasnotonlyinteresting butalsoservedtoin1buestudentsv-1ithasenseofthedynamic natureof taxonomy andthe development of our understanding of earn group.Unlessotherwiseindicated,theClassification section in each chapter deals only withextant taxa. Descriptions oftaxaintheseannotatedclassifications are written in somewhat telegraphic style to save space;,,ve neverexpectedthesesectionstobe"read"they are for reference.Important newwo1·ds,when firstdefined, aresetin boldfacetype.These boldfaced terms are alsoindicatedby boldfacedpagereferences intheindex;thustheindexcanalsobeusedasaglossary.Wetriedhardtobeconsistentinourusageofzoological terminology,buttheexistenceofsimilartern1s for entirelydifferentstructuresincertaingroupsisnotoriouslytroublesome-thesearenotedinthetext.
Forth.isSecondEditionofInvertebrates,ofcourse,we havetriedtobeascurrent aspossiblewiththeresearch literature,but even as thisbookgoesinto production important newpublicationsappeardaily. Ithas been estimated that the volumeofscientificinformationis doublingaboutevery10years(orfaster).Ahalf-million nonclinicalbiologypapersarepublisheda11nua1Jy.As ProfessorGeorgeBartholome1..vnoted,"Ifoneequates ignorancewiththeratiobetweenwhat one knowsand whatisavailabletobeknown...each biologicalinvestigatorbecomesmoreignorantwitheverypassingday." Mygoalhas beentoprovidesufficientreferencematerialtoleadtheinterestedstudentquicklyintotheheart of therelevant literature.Mostof thereferences cited in thetextwillbefound at theend of thecorrespondmg chapter.However,to conservespaceandelin1mate redundancy,inanumber of cases(especiallyinfigure citations)references of a generalnaturemay belisted only once,usually inthe introductory chapters.You willalsonoticecitationsofafairnumberof references thatare quite old,somefromthenineteenthcentury. These are included not out of whimsy, but because manyofthesearebenchmarkresearchpapersorthey standout as so.meof the best available descriptions
forthesubject at hand.(ltissurprising howmany of theillustrationsinm.odern biologytextscan betraced backtoorigins in nineteenth-centurypublications.) It isdistressingtoseehowcommonplaceithasbecon1e forresearcherstoignoretheexcellent(andimportant) workofpastdecades.For example,manyphylogenetic research paperscompletelyignore 150yearsofcareful embryologicalresearc11that was published,largelym theGermanandAmericanliteratLtre,inthenineteenth and twentiethcenturies.Forsomescientists, biological researchseemstobelittlemore than"sound bites" from thepastdecade.Sadly,today,this"soundbiteresearc11culture" is oftenimbuedingraduatestudentsa shocking and dangeroustrendthat encouragesdilettantes.To understandanimalsrequires a thorough w1derstandingoftheiroverall biology,andthededicationofacareer,notjustdabbling.
Smeethe firsteditionofthisbook,therehasbeenan explosion ofresearchinthefieldofmolecularbiology. Muchofthishasbeeninmolecular phylogenetics,but hugestrides arealsobeingmadein theareaofmoleculardevelopmentalbiology.Papersin thesefieldsno1,v appearat sumapacethatitis difficulttowriteabout then1inatextbook,forfeartheideasvviJJbeobsoletein sixmonths.Therehavebeen1nanyne,-vphylogenetic hypothesesproposed on thebasis ofDNAsequence analyses smce the fistedition ofthis book. Many of the molecularphylogenetictreesthat werepublished before2000 were quirky andtroublesome, due tothe simple fact that the field is still new andemerging. Becausemostofthesetreesarerelativelynewandstill await rigorous testingwith independentdata,1,vedo not discussthen1 all. However,we dodiscussmolecular-based hypothesesthat have a growing body of support orhave receivedwidespreadattention.But,in generalwehavetakenaconservativeapproachinthis regard-weareonlyjust beginning to discover which genes are appropriate for differentlevelsofphylogeneticai1alysis, ai1dhowbest toanalyzethem.
These thingsbeingsaid,I hopeyou arenow ready toforgeaheadin yourstudyof invertebrates.Thetask mayatfirstseemdaunting,andrightly so.Ihopethat thisbookwillmakethisseeminglyoverwhelmingtask a bitmoremanageable.IfIsucceedinenhanciJ1gyour enjoymentandappreciationofinvertebrates,thenmy effortswillhavebeenworthwhile.
R.C.B. Tucson,Arizona
Dece,nber2002
Acknowledgments
ThiseditionofInvertebrateshasagainbenefittedgreatly fromconscientiousreviewsprovidedbymanyspecialists, and we extend to these wonderful professionals ourutmost gratitude.Avery specialnoteof appreciationgoestoGonzaloGiribet,whonotonlyrevisedseveralchaptersandsectionsforthisedition,butalso graciously tookthetimeto reviewseveralother chapters; amoreinformed invertebrate zoologistdoes not exist todayandv,edeeply appreciatethehelpheprovided. Rebecca Rundellread theentire text-adaunting undertaking-providingcriticalscientificandinstructororientedfeedback;wewerefortunatethatshewaswillingtoundertakethisformidabletaskandwethankher profusely! Other colleagueswhowentabove and beyondin providingassistanceincludeLarryJonFriesen, JensH0eg,ReinhardtKristensen,BrianLeander,Sally Leys, ClausNielsen, andMartin S0rensen, to whom we owea great debt ofgratitude.Larry Friesen's photographiccontributions to thiseditionofinvertebrates tremendously enhanced thebook.
Invertebratesis in fourlanguagesand enjoysabroad readership,especially inEurope andLatinAmerica. Many students havewritten over the yearsexpressing theirsupport and encouragement and sending
photographsorothermaterial,especially fromMexico and South A1nerica, butnone hasbeen ascreativeor inspirationalasLorenaVianaandherfriendsfro1nthe UniversityofSaoPaulo.M11itoobrigado,Lorena.
Most of the original artworkin thistext was done fro1n our own sketches orfromother sources by the award-winningscientificillustratorNancyHaver,supportedby ourpublisher,SinauerAssociates.Wehave been incrediblyfortunatetohaveNancyworkingwith uson allthreeeditionsoflnvertebrates.ThehighlytalentedproductionstaffatSinauerhasahvaysbeenajoy towork with, and forthis editionweonce again had theskillsofJaniceHolabird,MarthaLorantos, David McIntyre,MarieScavotto,andChrisSmall.We areespecially gratefultoProductionEditorMarthaLorantos, who led the team for this edition, doing so withextraordinarytechnicalskill,patience,andgoodhumor. Marthasomehow n1anaged to keep this locomotive on thetracks no1natter how many twists,turns, and switchesit took. Andy Sinauer has been part ofthis project sincethernid-1980s, andhehasbeen unwaveringinhiswise council,patience,and greatinsight.We are deeplyindebtedtoAndyforhisconsistentsupport andpersonalinterestinthistextthroughoutitshistory. Asa book publisher(and booklover)Andy'sdedicationtoqualityand professionalismisunequaled.
GuestContributors
Jesus Benito, He1njchordata (with Fernando Pardos), Universidad Complutense, Madrid, Spain
C. Sarah Cohen, Urochordata, CaliforniaState University at San Francisco,California,USA
Gonzalo Giribet,Onychophora, Nen,ertea, Chelicerata (with Gustavo Hormiga), Annelida: Sipuncula, Metazoan Phylogeny (withRichard C. Brusca), Museum of Comparative Zoology, Harvard University, Cambridge, Massachusetts, USA
Rick Hochberg, Gastrotricha, University of Massachusetts Lowell, Lowell, Massachusetts, USA
Gustavo Hormiga, Chelicerata(with Gonzalo Giribet), The GeorgeWashingtonUniversity, Washington, DC, USA
Reinhardt M0bjerg Kristensen, Tardigrada (with Rjchard C. Brusca), Loricifera, Micrognathozoa (with Katrine Worsaae),NaturalHistory Museum of Denmark, University of Copenhagen, Copenhagen, Denmark
David Lindberg, Mollusca (with Winston Ponder andRichard C. Brusca), University of California, Berkeley,California, USA
Carsten Li.iter, Brachiopoda, Museum fi.ir Naturkunde, Berlin, Germany
Joel W. Martin, Crustacea (withRichard C. Brusca), Natural History Museum of Los Angeles County, Los Angeles,California, USA
Alessandro Minelli, Myriapoda, University of Padova, Padova, Italy
Rjch Mooi,Echinodern1ata, California Academy of Sciences,San Francisco, California,USA
Ricardo Cardoso Neves,Cycliophora, Biozentrurn, University of Basel, Basel, Switzerland
Claus Nielsen, Entoprocta, Bryozoa, Natural History Museun1 of Denmark, University of Copenhagen, Copenhagen, Denmark
Fernando Pardos, Hemichordata (vvithJesus Benito), Universidad Complutense, Madrid, Spain
Winston Ponder, Mollusca (with David Lindberg and Richard C. Brusca), Australian Museum, Sydney, Australia
GregRouse, Annelida: non-Sipuncula, Scripps Institution of Oceanography, University of California, SanDiego, California,USA
Scott Santagata, Phoronida, Long Island University, Greenvale, New York, USA
Andreas Schmidt-Rheasa, Nematomorpha, ZoologicalMuseum, University of Hamburg, Germany
George Shinn, Chaetognatha, Truman State University, Kirksville, Missouri, USA
Martin Vinther S0rensen, Kinorhyncha, Priapula, Gnathostomulida,Rotifera, Natural History Museum of Denmark, University of Copenhagen, Copenl1agen, Denmark
S. Patricia Stock, Ne1natoda, University of Arizona, Tucson, Arizona, USA
Katrine Worsaae, Micrognathozoa (vvithReinhardt M0bjerg Kristensen), University of Copenhagen, Denmark
Chapter reviewers for the Third Edition include the following:
Nicole Boury-Esnault,VlaamsInstituut voor de Zee, Oostende, Belgium
Jose Luis Carballo, Universidad Nacional Aut6noma de Mexico, Estacion Mazatlan, Mexico
Allen Collins, SmithsonianInstitution, Washington, D.C.
Alexander V. Ereskovsky, French National Center for Scientific Research, Institut Mediterraneen de Biodiversite et d'Ecologie Marine et Continentale (IMBE), Marseille, France.
Daphne G. Fautin, Professor Emerita, University of Kansas, Lawrence, USA
Gonzalo Giribet, Harvard University, Ca,nbridge, Massachusetts, USA
Gordon Hendler, Natural History Museumof Los Angeles County, Los Angeles,USA
Jens H0eg, University of Copenhagen, Denmark
Matthew Hooge, University of Maine, Orono, USA
Michael N. Horst, Mercer University, Georgia, USA
Michelle Kelly, NIWA (National Institute of Water and Atmospheric Research), New Zealand
KevinKocot, University of Alabama, Tuscaloosa, USA
Reinhardt Kristensen, University of Copenhagen, Denmark
Christopher Laumer,Harvard University, Cambridge, Massachusetts, USA
Brian Leander, University ofBritish Columbia, Vancouver, Canada
Sally Leys, University of Alberta, Edmonton, Canada
Renata Manconi,Universita degli Studi di Sassari (UNlSS), Italy
Mark Q. Martindale, Director, Whitney Laboratory and Seahorse Key Marine Laboratory, and Professor ofBiology, University of Florida, Gainesville, USA
Rick McCourt, Academy of Natural Sciences, Philadelphia,USA
Catherine S. McFadden, Harvey Mudd College, Clare,nont, California, USA
Claus Nielsen, University of Copenhagen, Denmark
David Pawson, National Museum of Natural History, Smithsonian Institution, Washington, DC, USA
Hilke Ruhberg, University ofHamburg, Germany
Rebecca Rundell, State University of New York-ESF, Syracuse, New York,USA
Jean Vacelet, Universite de la Mediterranee AixMarseille, France
R. W. M. van Soest, University of Amsterdam, The Netherlands
Media and Supplements to accompany Invertebrates, Third Edition
eBook
Invertebrates,ThjrdEditionis availablefor purchase asaneBook,inseveraldifferentfonnats,includingVitalSource,Yuzu,BryteWave,andRedShelf.TheeBook can be purchased aseither a180-day rental or a permanent(non-expiring)subscription. Allmajormobile devices are supported.For details on the eBook platformsoffered, please visitwv.,w.sinauer.com/ebooks.
FortheInstructor
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Instructor's Resource Library
TheInvertebrates,ThirdEditionInstructor'sResource Libraryincludes an extensive collection of visual resourcesforuseinpreparinglecturesandothercourse materials.The IRLincludesthefollowing:
TextbookFiguresandTables:Allofthetextbook'sfigures andtablesare includedasbothhjgh-andlow-resolutionJPEGs,foreasy useinpresentationsoftware, learning management systen,s, and assessments. New for theThudEdition, trus nowincludesall of thetextbook'sphotographs.
Supplen1entalPhotoCollection: Expandedfor theThird Edition,thjs collection of over 1,000 photographs depicts organisms that span the entire range of phylacoveredin the textbook.
PowerPointPresentations:Twoready-to-usePowerPoint presentationsareprovidedfor eachchapter of the textbook: one that containsall ofthetextbook figures andtables,andonethatcontainsalloftherelevantphotosfromthesupplementalphotocollection.
he incredible array of extant (= living) invertebrate species on Earth is the outcomeofhundredsofnullions of years of evolution. Indirect evidenceof the first life on Earth, prokaryotic organisms, has been found in some of the oldest sedimentary rocks on the planet, suggesting that life first appeared in Earth's seas almost as soon as the planet cooled enough for it to exist. TheEarth is 4.57billion years old, and the oldest rocks found so far are about4.3 billion years old. Although the precise date of the first appearance of life onEarth remains debatable, there are tantalizing 3.8-billion-year-old trace fossils fron1 Australia that resemble prokaryotic cells although these have been challenged, and opinion is now split on whether they are traces of early bacteria or sin1ply mineral deposits. However, good evidence of prokaryotic life has been found in pillow lavathat formed on the seabed 3.5 billion years ago, now exposed in South Africa. And3.4-billion-year-old fossil cells(probablysulfur bacteria) have been found an1ong cemented sand grains on an ancient beach in Australia.1
The next big step in biological evolution came about when prokaryotic cells bega11 taking in guests. Around 2 to2.5 billion years ago, one of these primitive cellstook in a free-living bacterium that established permanent residency, giving rise to the organelles \Ve call mitochondria and thiswas the origin of the eukaryotic cell. Mitochondria, you will recall, generate energy for their host ceils by oxidizing sugars, and in this case they also equipped early life to survive in Earth's increasing oxygen levels. Evidence suggeststhat nutochondriaevolvedjust once, from a
TABLE1.1 Numbers ofDescribed Living Species inthe 32 Animal syn1biotic a-proteobacterium, Phyla (-1,382,402total; -1,324,402, or96% are and then subsequently diversiinvertebrates)8 fiedbroadly. Modernfree-Jiving relativesof thisbacterium harbor
Number of Percent ofTota about 2,000 genesacross several Described DescribedAnimal Taxon Species Species millionbases,buttheir1nitochond.rialdescendantshavefarfewer, PhylumPorifera
9000 0.65 sometin1esasfewasthree genes.
Phy umPlacozoa 1(or2) 0.0001 Andhumanmitochondrial DNA
PhylumCnidaria
13,200 0.95 harborsonlyabout 16,000bases. On the other hand, so1ne plants Phy umCtenophora
PhylumXenacoelomorpha
Phy umPlatyhelminthes
100 0.007 have greatly expanded theirmi-
400 0.03 tochondrial genome, the largest
26,500 1.92 so far discovered in the genus Silene, with around 11 million PhylumChaetognatha 130 0.009 bases. Another prokaryotic intraPhyumGastrotricha
800 0.06 cellularguest, acyanobacterium,
PhylumRhombozoa (=Dicye,nida) 70 0.005 became the ancestor of chloroplaststhroughthesan1esymbioPhy umOrthonectida 21 0.002 genie process; chloroplasts, of
PhylumNemertea 1300 0.09 course, are the photosynthesiz-
PhylumMollusca
5.79 ing organelles that made plants and algaepossible.Insomepla11t
PhylumAnnelida 20,000 1.45 and algae Jilles,the origillal chloPhy umEntoprocta 200 0.014 roplastwaslost,and a new one
Phy umCycliophora 2 0.0001 waspicked up vvhen a host cell took in an alga and co-opted its
PhylumGnathostomulida 100 0.007 chloroplast in another kind of
PhylumMicrognathozoa 1 0.0001 symbiogenicevent(seeChapter3 for a detaileddiscussion of these PhylumRotifera
bio1narkerssuggest that thefirst eukaryoticcellsmight have ap- Phy umBrachiopoda
0.03 peared as early as 2.7 billion
Phy umNematoda(=Nemata)
years ago (late Archean), alPhy umNematomorpha
0.03 though the earliest fossils that have been proposed to be euPhylumKinorhyncha
PhylumPriapula
PhylumLoricifera
PhylumTardigrada
PhylumOnychophora
0.014 karyotes-based on cell surface
0.001 features and theirlargesize-are
0.003 about 1.8 billion years old (early Proterozoic). Multicelled algae
0.087 (protists) date as far back as 1.2
0.014 billion years. Eukaryote-likemicrofossils have been described
PhylumArthropoda from 1-billion-year-oldfreshwa-
SubphylumCrustacea
ter deposits, suggesting thatthe eukaryotes might have left the PhylumArthropoda sea and invaded the terrestrial SubphylumHexapoda
realm longago. Even though the PhylumArthropoda eukaryotic condition appeared earlyin Earth'shistory, it took a SubphylumChelicerata
fewhundredmillion more years
PhylumArthropoda for multicellular organisms to
Subphy umMyriapoda
PhylumArthropoda
firstevolve.
Disputed trace fossilshaveled
some to suggest that the earliest
TABLE 1.1 (Continued)
PhylumEchinodennata
PhylumHemichordata
PhyumChordata
SubphylumCephalochordata
Phylw11Chordata
SubphylumUrochordata
PhylumChordata
SubphylumVertebrata
PhylumChordataTOTAL
There is no argun1ent that
Described Animal Metazoa are n1onophyletic (i.e., a clade),andtheanimal kingdom is defined by numerous synapomorphies,including: gastrulation and en1bryonicgern1layer formation; unique modes of oogenesis and spermatogenesis; a unique sperm structure; mitochondrial gene reduction; epidermal epithelia withseptatejw1ctions, tight junctions, or zonula adherens; striate myofibrils; actin-myosin
315,000;andFungi=100000. lagen; andthepresenceof a basal lanli.na/basement membrane beneathepidermallayers(of course, some of these features have been secondarily lost in son1e groups).
animals (Metazoa)mighthaveoriginated a billion years ago, but recent n1oleculai· clock estimatesput the originofMetazoa at875 to650 million yearsago.Theoldest generally acceptedmetazoan fossils are from the Ediacaran period, found in the Fermeuse Formation of Nev-•foundland (-560 Ma) and the Doushantuo Formation of southernChina(600-580 Ma). A560-million-year-old likely cnidarian (namedHaootinq11adrifonnis) has been described from Newfoundland, with quadraradialsymmetry and clearly preservedbundled n1uscular fibers.Haootin appears to be a nearly 6-cmlong polyp, or perhaps an attached medusa-it re sembles modern speciesofStaurozoa.Cnidariansand otherapparent diploblastic animals have beenreported from theDoushantuodeposits, although these have been met with skepticistn in some quarters. However, in2015,aseemingly reliable600-million-year-oldfossil sponge(Eoci;nthispongiaqiania) was describedfrom the Doushantuo Formation.In 2009, Jun-Yuan Chen and colleagues reported on embryos ofreputed bilaterians (triploblasts) in the Doushantuodeposits (dated600580 Ma)-32-cellstage embryoswith micromeresand macromeres, apparent anterior-posterior and dorsoventra1patterning, and ectoderm-likecellsaroundpart of their periphery. This finding was challenged, and the fossils v-•ere variously declared as prokaryotesor protists byother workers. However, furtherdiscoveriesof additional embryos seemed to support the vie,-v of these being bilaterian embryos and, in some cases, perhaps diapause embryos ("restingeggs") of bilaterians. Good trace fossils (tracks) of aminute wormlike bilaterian animal, possibly with legs, have also been describedfrom585-million-year-old rocksinUruguay. These fossil records put the appearance of "higher metazoans" (i.e.,bilaterians) millions of years before the beginningoftheCambrian period.
Evidenceis strong that Metazoa arose out of the protist group Choanoflagellata, or a common ancestor, and the two comprisesister groups in aln1ost all recent analyses. They are,in turn, part of alarger clade known as Opisthokonta that also includes the fungi and several smallprotist groups(seeChapter3).
The three great lineages of life on Earth-Bacteria, Archaea, Eukaryota are very different from one another.Bacteria and Archaea havetheirDNAdispersed throughout thecell, whereas in Eukaryotathe DNA is enclosed within a membrane-bound nucleus. The cell lineages that gave rise to the Eukaryota are still wlknown.Themany millennia betweenthe origin of Eukaryota and theexplosiveradiation that apparently began in theEdiacaranissometimescalled the "boring billion years," but the fossil record is fairly sparse for that time period,so we'renot surehow "boring" it actuallywas. A popular hypothesissuggests that oxygen levelswere too low duringthat time for larger organismstoevolve (seebelow).
Today, thereare an estimated 2,007,702 described and named living species. About 58,000 of these are vertebratesand 1,324,402 are invertebrates(Table 1.1). Inaddition, about 200,000protists have beendescribed, 315,000 plants (290,000 seedplants),and 100,000 fungi. And 15,000 to 20,000 new species are described every year.It seemslikely thata significantportion of Earth's biodiversity, at the levelof both genes and species, resides inthe "invisible"prokaryotic world, and we have co1ne to realize howlittle weknow about thishidden world.About10,300species of prokaryotes have been described,but there areanestimated10 million (or perhaps more) undescribed prokaryote specieson Earth. An esti.n1ated 135,000 more plantspecies remain to be described. Overall, estimatesof undescribed eukaryotes range fromlows of 3-8million tohighsof 100 millionor more.
How can we possibly keep track of all these species names and information abouteach ofthe1n,andhow dowe organize them in a meaningful way? We do so withclassifications.Classificationsare listsof species, ranked in a subordinated fashion that reflects their evolutionary relationships and phylogenetic history. Classifications summarize the overarclling aspects of the tree of life.Atthe highest level of classification, we can recognize two superkingdon1s: Prokaryota (containing the kingdoms Archaea and Bacteria) and Eukaryota (containing the kingdo1ns Protista, Fungi, Plantae,andAnirnalia/Metazoa).Because"Protista"is not a monophyletic group,theprotists aresometimes broken up into several kingdon1s, or other classificatory ranks,buttherelationshipsamongtheprotistsare still beingdebated(seeChapter3).
Oneof the earliest and best-known evolutionary trees of life published from aDarwinian (genealogical) perspective wasbyErnst Haeckel in 1866(Figure 1.1).Haeckelcoined theterm"phylogeny," andhisfamoustrees codifiedwhat becameatraditionof depicting phylogenetic hypothesesasbranching diagrams, a traditionthathas persistedsince that time. However, ahand-drawn sketcl1 inCharles Dar\,vin's field notebook(1837)clearlydepictshisviewofSouthAmerican mammal evolution in a branchingtree of extant and fossil species. Andin hisbook, On the Origin ofSpecies (1859),Darwin presented ru1abstract branching diagra1n of a theoretical treeof speciesas a way of illustrating his conceptof descent with modification.Jean Baptistelan1arck probablypresented the firsthistorical trees ofaniJnalsinhisPhilosophieZoologiquein1809, and theFrench botanist AugustinAugierpublished a tree showing the relationships among plants in 1801 (perhaps thefirst treeeverpublished)-although both lan1arck's and Augier's trees were produced before themodernconceptofevolutionhadbeen clearlyarticulated.Wediscussvariousways inwhicllphylogenetic treesare developed in Chapter2. SinceHaeckel's day,many names have beencoined forthe branches that sprout from these trees, and in recent years a glut of new names hasbeen introduced to labelvarious molecu.Jarlybased cladesnestedwithin the tree of life. We \•viiinot burden you with all of thesenames,but afewofthemneedtobe definedhere before we launchinto ourstudy ofthe invertebrates. Some of these names refer to groups of organisms that are thought to be natural phylogenetic lineages
(i.e.,groups thatinclude all the descendru1tsofastem species, known as monophyletic groups,or clades). Exa1nplesofsucllnatural,or monophyleticgroups are thesuperkingdom Eukaryota, kingdom Metazoa (the animals), and kingdom Plantae(the lower and higher plru1ts).2 Allthree of theselargegroupingsare thought to have had a single origin,and theyeacll include aU of the species descended from that original ancestor. Monophyletic groups con1prise a cluster of tern'linal branches (with a single origin) embedded \,vithin a much largertree.Some other nan1ed groups arenatural, having asingleevolutionary origin, butthe group doesnotcontainnilofthe111e111bers of the lineage.Such groups are saidto be paraphyletic, andthey areoften the basal or ancestral lmeagesin a muchlargerclade. Paraphyletic groups comprise some, but not all descendants of a stemspecies.TheProtista are paraphyleticbecause thegrouping excludes three large multicelJed lineages that evolved out ofit (e.g.,Metazoa, Plantae, Fungi). Another well-known paraphyletic group is Crustacea (which excludes the Hexapoda/ lnsecta, a clade that evolved out of it). The clade that includes both Crustacea and Hexapoda is known as Pancrustacea. Classifications of life are derived fron1 evolutionary or phylogenetictrees, andthusgenerally include only monophyletic groups. However, son1etimesparaphyletic taxa are also used because, if they are unambiguous, they can beimportant in facilitating meaningful communication amongscientists and between the scientific community and society (e.g., ProtistaandCrustacea).
Some na1nes refer to unnatural, or co1nposite, groupmgs oforganisn1s,sucll as"microbes" (i.e., any organism that is microscopic in size, sucll as bacteria, archaeans, yeasts,unicellularfungi,andsomeprotists). These unnaturalgroups are polyphyletic. For example, yeasts are unicellular fungi that evolved several times independently from multicellular filamentous ancestors;today they areassignedto oneof threehigher fu11gal phyla, so theconceptof "yeast" represents a polyphyletic,orunnaturalgrouping. Thenan1e"slugs"
Mollus1·a Olc>(llrtli'a tl1u1! '' IGlf-�'-t �r-:;l!l, --:-t :\l'I1b� �•fs.u"· Ii. j '"'i'" rr,'�))ull}Uc\•:, h u;. /it,
Ilatlix · Monophylelischer �lont•l'l!S Stammbaum,1,rOrganismen 1 :mlog'Olllll'II m.11wjO,u,1tlqrJl'l·lt11t(,,,,J 11 ,· . t:01111UllltlS Or·g1ni�11rnr11ul X L�---�-�b.....,=�6=-�-�d----�===A t /:,r,,.,·t lla«l.�I.Je,,a l86'1i
1h
.rl��u..
animalc
(or "sea slugs") also refers to agroup ofanimalsthat do not share a single ancestry (the slug forn1 has evolved many times among gastropod1nolluscs), so slugs are polyphyletic (see chapter opener photo of aSpanish shawl slug, Flnbellinniodinen). We explore these concepts more fully inChapter2.
We know approximately how many genes are in organisms from yeast (about 6,000 genes) to humans (about 25,000 genes), but we don't knov.• how many living species inhabit ourplanet and the range in estimates is surprisingly broad. How many undescribed species are lingering out there, waiting for names?However derived, predictions of global species diversity rely on extrapolations from existing realdata. Methods of estimation have included rates ofpast species descriptions, expert opinion, the fraction of undescribed species in samples collected, and ratios between taxa in the taxonomic hierarchy. Each method has its limitations. Two recent estimates of undescribed marine animals (Mora et al. 2011 and Appeltans et al. 2012) reached the conclusion that 91% vs. 33-67% (respectively) of the world's eukaryotic marine fauna is stilJ undescribed. More recently, a large research program sampling the Western Australian upper continentalslope for Crustacea and Polychaeta found 95%of the species to beundescribed (with the rate of new species obtained by the sampling program not even leveling off). Given the vast extent of the poorly-sampled world's continental slopes, not to mention the deep sea, rainforests, and other littlesampled habitats, these data suggest that estimates of over 90% undescribed eukaryotes on Earth are not unreasonable.
Our great uncertainty about how many species of living organismsexist onEarthis unsettling andspeaks to the issue of priorities and funding in biology. At our current rate of species descriptions, it might take us 10,000 years ormore to describejustthe rest of Earth's eukaryotic life forms. Notall of the species remaining to be described are invertebrates between 1990 and 2002 alone, 38 new primate species were discovered and named. And if prokaryotes are thrown into this mix, thenumbers become even larger. Recent gene-sequencesurveys of the world'soceans (based largelyon DNA "barcodes"-16S ribosomal gene sequences for Bacteria and Archaea, 18S ribosomal gene sequences foreukaryotes) have revealed a massive undescribed biota of microbes in the sea. Similar discoveries have been made withgenetic searchesfor soil microbes. For example, there areabout30,000 forn1ally namedbacterial varietiesthatare in pure culture, but estimates of undescribed species range from 10 million to a billion ormore! Andv.•enow know thatthousands of bacterial species inhabit the human body, almost all of which arenot yet even namedanddescribed.Viruses still lack auniversal molecularidentifier, and theworldscopeof viral biodiversity is essentiallyunknown.
There are currently several atte1npts to compile a List of all known species on Earth. The United States Geological Service (USGS) hosts ITIS-the Integrated Taxonomic Information System. The goal of!TIS is to create an easily accessible database ,.vith reliable inforn1ation on species nan1es and their classification. Recently, ITIS and several other initiativesturnedtheir data over to the Catalogue of Life(Col) project, which is building the species list (up to 1.5 million species as this book went to press) and maintaining a "consensus classification" of all life (see www.catalogueof life. org, andRuggiero et al.2015).TheEncyclopediaof Life (EOL) project is building a website that offers not just species names, but also ecological information about each species; it currently contains more than 175,000 vetted species pages. WoRMS(The World Register of Marine Species), an open-access online database \Vith the goal of listing all described eukaryotic marine species, predicts the con1pleted inventory will catalog 222,000 to230,000 species.
However, at our current rate of anthropogenically driven extinction a majority of Earth's species will go extinct before they are ever described. In the Unjted States alone, at least 5,000 nan1ed species are threatened with extinction, and an estimated 500 known species have already gone extinct since people first arrived in North America. Globally, the United Nations Environn1ent Programme estimates that by 2030 nearly25% of the world's mammalscould go extinct, and recentcountsindicate 322 vertebrate species have already become extinct since 1500. Some v.,orkers no,,v refer tothe time since the start of the Industrial Revolution as theAnthropocene--a period n1arked by humanity'sprofoundglobal transformation of the environment. Morethan halfof Earth'sterrestrial surface is now plowed, pastured, fertilized, irrigated, drained, bulldozed, compacted, eroded, reconstructed, mined, logged, or otherwise converted to new uses. Humandriven deforestation removes15 billiontrees per year. E. 0. Wilson once estimated that about 25,000 species are goiJ1g extinctannually on Earth (v.re just don't know what theyare!).
Pimm et al. (2014) calculated extinction rates as fractions of species going extinct over time-extinctions pernilllion species-years(E/MSY). For exan1ple, 1,230 birdspecies have beendescribed since1900, and 13 of these are nowextinct. This cohort accun1ulated 98,334species-years, meaning an average species has been known for 80 years. The extinction rate is thus 13/98,334 x 106 = 132 E/MSY. They calculated that, beforeHo1nosapiens arrived on the scene, the overall background animal extinction rate was 0.1 E/MSY; today itis aboutJOOE/MSY(a thousand times higher). ProportionalJy speaking, larger animals (e.g., vertebrates), higher in the foodchain andfev.•er in number, are more likely to go extinct than invertebrates. This means invertebrates(and protists),which already run
Even thoughinvertebratesmake up96% of the described animal kingdom(Table1.1),they account for amere 38%ofthe500orsospecies now under protection bytheU.S.EndangeredSpeciesAct.NatureServe has argued that more than 1,800 invertebrate species need protection, ,,vhile the IUCN Red List of Threatened Species documents the extinction risk of nearly50,000species of animals and plants. In2002, theU.N.Conventionon BiologicalDiversitycommittednationstosignificantlyreduceratesofbiodiversity loss by 2010, and in2010this call wasrenewed•,,vith aset of specific targetsfor2020.However,several recentstudieshaveshown thattheconventionhassofar failed and rates ofbiodiversity loss donot appear to beslowingatall.Further,the Conventionhascrippled scientific fieldwork around the1vorldby instilJingin many nations a fear ofoutside researchers"stealing their geneticbiodiversity."
Thesinglegreatestthreattospecies survivalforthe past200yearshas been habitatloss.Although wehear mostly about deforestation,30 to50% of theEarth's coastalenvirorunentshave beendegradedduringpast decades,atratesexceedingthoseoftropicalforestloss. Looking forward,thedamaging effectsof habitatloss will likely be matched (and escalated) byanthropogenically-drivenglobal clin1atechange.Theconcentrationofcarbondioxide(CO2) inEarth'satmospherehas risenbyabout 38%sincethe startoftheindustrialera as a resultof fossil fuel burningandlandusechange, and aquarterto athirdofallthe CO2e1nittedthrough human activitieshas been absorbed by theocean, resulting in acidification ofsurface waters. In fact, the oceans overall are novv about30%more acidic than theywere100yearsago. ThedropinoceanpHiscreatinghardshipson animalswithcalciumcarbonateskeletons,anddamagehasbeendocumentedineverything from coralsto sea butterflies (pteropodmolluscs). In May2013,theconcentration of CO2intheatn1osphere reached400ppm,the highesti.thas beenover thepast 2tnillionyears.Neverbefore hassucharapidglobalscaleincreaseinCO2(andtemperature)occurredduring thehistory ofhumancivilization. Rising concentrations of greenhouse gassesin the atmosphere are leadingtoincreasingglobaltemperaturesandchanges inprecipitationregimes,andthesechangesarein1pactingthedistribution ofbiota acrosstheplanet.Globally, averageairtemperatureshaverisen about0.8°Csince 1880, mean land surface temperature has warmed 0.27°Cper decade since 1979,and projections from globalclin1atemodelspredict globalatmospherictemperaturesto increase by about4°C by theend of this century.Meltingpolariceand glaciers,combined1-vith expansion of •,,vanning ocean vvaters, are driving up sea level,whichisexpectedtobeasmuchasfourfeet higherbytheendof thiscentury.
Prokaryotes and Eukaryotes
The discoverythatorganisms witha cellnucleusconstituteanatural(monophyletic)groupdividedtheliving world neatly into twocategories,the prokaryotes (Archaea and Bacteria:thoseorganismslackingmembrane-enclosed organelles and anucleus,andwithout linearchromosomes),andthe eukaryotes(thoseorganisn1s that dopossess men1brane-bound organelles, a nucleus,and linearchromosomes). Investigations by CarlWoeseand others,beginningin the 1970s,ledto thediscovery thattheprokaryotesthemselvescomprise two distinctgroups,calledBacteria(=Eubacteria)and Archaea (= Archaebacteria), both quite distinctfrom eukaryotes(BoxlA).Bacteria correspondmoreorless toour traditional understanding of bacteria. Archaea strongly resemble Bacteria,butthey have genetic and n1etaboliccharacteristics thatmakethem quiteunique. For exan1ple, Archaea differfrom bothBacteria and Eukaryotain thecomposition of their ribosomes, in theconstructionof their cell walls, and in the kindsof lipids in their cellmembranes.Some Bacteriaconduct chlorophylJ-based photosynthesis,atrait that isnever present in Archaea (photosynthesis is the harvesting of lightto produce energy/sugars and oxygen). Current thinkingfavors the viev., thatprokaryotesruled Earth forabout a billion years before the eukaryotic cell appeared.
As the prokaryotes evolved,they adapted tocolonize everyconceivableenvironmentonEarth.During the early evolution of prokaryotes, Earth's airhad almostnooxygen,consistingprimarilyofCO2,1nethane, and nitrogen. The n1etabolismof the earliest prokaryotesreliedon hydrogen,methane,andsulfur,anddid notproduceoxygen asabyproduct.ltwastheappearance ofthe first oceanicphotosynthesizingprokaryotes thatled to increased atmosphericoxygenconcentrations,settingthe stagefor theevolutionofcomplex multicellular life.And aquatic species v.,ereprobably ableto colonizelandonly because the oxygen helped create theozonelayerthat shieldsagainstthesun's ultravioletradiation.Just whenoxygen-producingphotosynthesis beganisstillbeingdebated,but whenit happened,mostoftheearlychemoautotrophicprokaryotes werelikelypoisonedbythe "newgas"intheenvironment. Alargebody ofevidencepointstoasharprisein theconcentration of atmosphericoxygenbetween2.45 and2.32billionyearsago(thisissometimescalled the "greatoxidation event"),aroundthesametimetheeukaryoticcellfirstappeared.Thisevidenceincludesred bedsor layerstingedbyoxidizediron(i.e.,rust)andoil biomarkersthat may be there1nainsofCyanobacteria (true Bacteria). However, in western Australia, thick shaledepositsthat are3.2billionyearsoldhavebacterial remains thathintatoxygen-producingphotosynthesis.Theseancientoxygenlevelsmighthavereamed around40% of present atmospheric levels. There is
alsoevidence in the geologicalrecord that atmospheric oxygendid not steadily increase,but fluctuated vvi.ldly, dropping at times to a mere 0.1% of current levels. It may not have been until around 800 million years ago thathigh oxygenlevelsstabilized.
Terrestrial photosynthesis haslittle effect onatmospheric 02 because it is nearly balanced by the reverse processes of respiration and decay. By contrast, marine photosynthesis is a net source of02 because a small fraction (~0.1%) of the organic matter synthesized in the oceans is buried in sediments. It is this small "leak" in the marine organic carbon cycle is responsible for most of our atmospheric 02. Cyanobacteria are thought to have been largely responsible for the initial rise of atmospheric02 onEarth, andeventoday Prochlorococc11s can be the numerically dominant
phytoplankter in tropical andsubtropical oceans, accounting for 20 to 48% of the photosynthetic biomass and production in some regions. Today most marine photosynthesis is performed by Cyanobacteria and single-celled protists, such as diatoms and coccolithophores. Cyanobacteria are nearly unique a1nong the prokaryotes in performing oxygenic photosynthesis, often together with nitrogen fixation, and thus they are major primary producers in both marine and terrestrialecosystems.
Many Archaea live in extreme environments, and thispattern is often interpreted as a refugial lifestyle-in otherwords,such creaturestend to livein placeswhere theyhavebeenabletosurvivewithoutconfrontingdangerous environments orcompetition from more highly derived life forms. Many of these"extremophiles'' are
