Introduction - WordPress.com · 2012. 10. 18. · INTRODUCTION 3 Figure 1.1 Haeckel’s Tree of...

ne of the first evolutionary trees of life conceived from a Darwinian(genealogical) perspective was published by Ernst Haeckel in 1866

(Figure 1.1). Haeckel’s famous tree of life began a tradition of depictingphylogenetic hypotheses as branching diagrams, or trees, a tradition that has per-sisted since that time. We discuss various ways in which these trees are devel-oped in Chapter 2. Since Haeckel’s day, many names have been coined for thelarger branches that sprout from these trees. We will not burden you with all ofthese names, but a few of them need to be defined here, before we launch into ourstudy of the invertebrates. Some of these names refer to groups of organisms thatare probably natural phylogenetic groups (i.e., groups that include an ancestorand all of its descendants), such as Metazoa (the animal kingdom). Other namesrefer to unnatural, or composite, groupings of organisms, such as “microbes”(i.e., any organism that is microscopic in size, such as bacteria, most protists, andunicellular fungi) and “protozoa” (a loose assemblage of primarily unicellularheterotrophic eukaryotes).

The discovery that organisms with a cell nucleus constitute a natural group di-vided the living world neatly into two categories, the prokaryotes (those organ-isms lacking membrane-enclosed organelles and a nucleus, and without linearchromosomes), and the eukaryotes (those organisms that do possess membrane-bound organelles and a nucleus, and linear chromosomes). Investigations by CarlWoese and others, beginning in the 1970s, led to the discovery that the prokary-otes actually comprise two distinct groups, called Eubacteria and Archaea (=Archaebacteria), both quite distinct from eukaryotes (Box 1A). Eubacteria corre-

Introduction

For a gentleman should know something of invertebrate zoology, call it culture or what you will,just as he ought to know something about paintingand music and the weeds in his garden.Martin Wells, Lower Animals, 1968

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spond more or less to our traditional understanding ofbacteria. Archaea strongly resemble Eubacteria, but theyhave genetic and metabolic characteristics that makethem unique. For example, Archaea differ from bothEubacteria and Eukaryota in the composition of their ri-bosomes, in the construction of their cell walls, and inthe kinds of lipids in their cell membranes. SomeEubacteria conduct chlorophyll-based photosynthesis, atrait that is never present in Archaea. Not surprisingly,due to their great age,* the genetic differences among

prokaryotes are much greater than those seen amongeukaryotes, even though these differences do not typi-cally reveal themselves in gross anatomy. Current think-ing favors the view that prokaryotes ruled Earth for atleast 2 billion years before the modern eukaryotic cellappeared in the fossil record. In fact, it seems likely thata significant portion of Earth’s biodiversity, at the levelof both genes and species, resides in the “invisible”prokaryotic world. About 4,000 species of prokaryoteshave been described, but there are an estimated 1 to 3million undescribed species living on Earth today.

Evolutionary change in the prokaryotes gave rise tometabolic diversity and the evolutionary capacity to ex-plore and colonize every conceivable environment onEarth. Many Archaea live in extreme environments, andthis pattern is often interpreted as a refugial lifestyle—inother words, these creatures tend to live in places wherethey have been able to survive without confronting

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*The date of the first appearance of life on Earth remains debat-able. The oldest evidence consists of 3.8-billion-year-old trace fos-sils from Australia, but these fossils have recently been chal-lenged, and opinion is now split on whether they are traces ofearly bacteria or simply mineral deposits. Uncontestable fossilsoccur in rocks 2 billion years old, but these fossils already includemulticellular algae, suggesting that life must have evolved wellbefore then.

THE PROKARYOTES (the “domains” Eubacteria and Archaea)a

Kingdom Eubacteria (Bacteria)The “true” bacteria, including Cyanobacteria (or blue–green algae) and spirochetes. Never with membrane-enclosed or-ganelles or nuclei, or a cytoskeleton; none are methanogens; some use chlorophyll-based photosynthesis; with peptidogly-can in cell wall; with a single known RNA polymerase.

Kingdom Archaea (Archaebacteria)Anaerobic or aerobic, largely methane-producing microorganisms. Never with membrane-enclosed organelles or nuclei, or acytoskeleton; none use chlorophyll-based photosynthesis; without peptidoglycan in cell wall; with several RNA polymerases.

THE EUKARYOTES (the “domain” Eukaryota, or Eukarya)Cells with a variety of membrane-enclosed organelles (e.g., mitochondria, lysosomes, peroxisomes) and with a membrane-enclosed nucleus. Cells gain structural support from an internal network of fibrous proteins called a cytoskeleton.

Kingdom FungiThe fungi. Probably a monophyletic group that includes molds, mushrooms, yeasts, and others. Saprobic, heterotrophic,multicellular organisms. The earliest fossil records of fungi are from the Middle Ordovician, about 460 mya. The 72,000 de-scribed species are thought to represent only 5–10 percent of the actual diversity.

Kingdom Plantae (= Metaphyta)The multicellular plants. Photosynthetic, autotrophic, multicellular organisms that develop through embryonic tissue layer-ing. Includes some groups of algae, the bryophytes and their kin, and the vascular plants (about 240,000 of which are flow-ering plants). The described species are thought to represent about half of Earth’s actual plant diversity.

Kingdom ProtistaEukaryotic single-celled microorganisms and certain algae. A polyphyletic grouping of perhaps 18 phyla, including eu-glenids, green algae, diatoms and some other brown algae, ciliates, dinoflagellates, foraminiferans, amoebae, and others.Many workers feel that this group should be split into several separate kingdoms to better reflect the phylogenetic lineagesof its members. The 80,000 described species probably represent about 10 percent of the actual protist diversity on Earthtoday.

Kingdom Animalia (= Metazoa)The multicellular animals. A monophyletic taxon, containing 34 phyla of ingestive, heterotrophic, multicellular organisms.About 1.3 million living species have been described; estimates of the number of undescribed species range from lows of10–30 million to highs of 100–200 million.

aPortions of the old “Kingdom Monera” are now included in the Eubacteria and the Archaea. Viruses (about 5,000 described“species”) and subviral organisms (viroids and prions) are not included in this classification.

BOX 1A The Six Kingdoms of Life


competition with more highly derived life forms. Manyof these “extremophiles” are anaerobic chemoauto-trophs, and they have been found in a variety of habi-tats, such as deep-sea hydrothermal vents, benthic ma-rine cold seeps, hot springs, saline lakes, sewagetreatment ponds, certain sediments of natural waters,and the guts of humans and other animals. One of themost astonishing discoveries of the 1980s was that ex-tremophile Archaea (and some fungi) are widespread inthe deep rocks of Earth’s crust. Since then, a communityof hydrogen-eating Archaea has been found living in ageothermal hot spring in Idaho, 600 feet beneath Earth’ssurface, relying on neither sunshine nor organic carbon.Other Archaea have been found at depths as great as 2.8km, living in igneous rocks with temperatures as highas 75°C. Extremophiles include halophiles (which growin the presence of high salt concentrations), ther-mophiles and psychrophiles (which live at very high orvery low temperatures), acidiphiles and alkaliphiles(which are optimally adapted to acidic or basic pH val-ues), and barophiles (which grow best under pres-

sure).* Molecular phylogenetic studies now suggest thatsome of these extremophiles, particularly the ther-mophiles, lie close to the “universal ancestor” of all lifeon Earth.

It has recently been suggested that the three main di-visions of life (Eubacteria, Archaea, Eukaryota) shouldbe recognized at a new taxonomic level, called domains.However, fundamental questions remain about thesethree “domains,” including how many natural groups(kingdoms) exist in each domain, whether the domainsthemselves represent natural (= monophyletic) groups,and what the phylogenetic relationships are amongthese domains and the kingdoms they contain. Currentevidence suggests that eukaryotes are a natural group,defined by the unique trait of a nucleus and linear chro-mosomes, whereas Eubacteria and Archaea may not benatural groups.

Courses and texts on invertebrates often include dis-cussions of two eukaryotic kingdoms, the Animalia (=Metazoa) and certain “animal-like” (i.e., heterotrophic)protist phyla loosely referred to as “protozoa.” Follow-ing this tradition, we treat 34 phyla of Metazoa and 18phyla of protists (many of which have traditionally beenviewed as “protozoa”) in this text. The vast majority ofkinds (species) of living organisms that have been de-scribed are animals. The kingdom Animalia, orMetazoa, is usually defined as the multicellular, inges-tive, heterotrophic† eukaryotes. However, its memberspossess other unique attributes as well, such as anacetylcholine/cholinesterase-based nervous system,special types of cell–cell junctions, and a unique familyof connective tissue proteins called collagens. Over amillion species of living animals have been described,but estimates of how many living species remain to bediscovered and described range from lows of 10–30 mil-lion to highs of 100–200 million.‡ Among the Metazoaare some species that possess a backbone (or vertebralcolumn), but most do not. Those that possess a back-bone constitute the subphylum Vertebrata of the phy-lum Chordata, and account for less than 5 percent(about 46,670 species) of all described animals. Those

INTRODUCTION 3

Figure 1.1 Haeckel’s Tree of Life (1866).

*One of the most striking examples of a thermophile is Pyrolobusfumarii, a chemolithotrophic archaean that lives in oceanichydrothermal vents at temperatures of 90°–113°C. (Chemo-lithotrophs are organisms that use inorganic compounds as energysources.) On the other hand, Polaromonas vacuolata grows optimal-ly at 4°C. Picrophilus oshimae is an acidiphile whose growth opti-mum is pH 0.7 (P. oshimae is also a thermophile, preferring tem-peratures of 60°C). The alkaliphile Natronobacterium gregoryi livesin soda lakes where the pH can rise as high as 12. Halophilicmicroorganisms abound in hypersaline lakes such as the DeadSea, Great Salt Lake, and solar salt evaporation ponds. Such lakesare often colored red by dense microbial communities (e.g.,Halobacterium). Halobacterium salinarum lives in the salt pans of SanFrancisco Bay and colors them red. Barophiles have been foundliving at all depths in the sea, and one unnamed species from theMariana Trench has been shown to require at least 500 atmos-pheres of pressure in order to grow.†Heterotrophic organisms are those that consume other organismsor organic materials as food.


that do not possess a backbone (the remainder of thephylum Chordata, plus 33 additional animal phyla)constitute the invertebrates. Thus we can see that thedivision of animals into invertebrates and vertebrates isbased more on tradition and convenience, reflecting adichotomy of zoologists’ interests, than it is on therecognition of natural biological groupings. About10,000 to 13,000 new species are named and describedby biologists each year, most of them invertebrates.

Where Did Invertebrates Come From?The incredible array of extant (= living) invertebrates isthe outcome of billions of years of evolution on Earth.Indirect evidence of prokaryotic organisms has beenfound in some of the oldest sediments on the planet,suggesting that life first appeared in Earth’s seas almostas soon as the planet cooled enough for it to exist.§ A re-markable level of metabolic sophistication had beenachieved by the end of the Archean eon, about 2.5 bil-lion years ago. Hydrocarbon biomarkers suggest thatthe first eukaryotic cells might have appeared 2.7 bil-lion years ago. However, we know very few detailsabout the origin or early evolution of the eukaryotes.Even though the eukaryotic condition appeared earlyin Earth’s history, it probably took a few hundred mil-lion more years for evolution to invent multicellular or-ganisms. Molecular clock data (tenuous as they are)suggest that the last common ancestor of plants and an-imals existed about 1.6 billion years ago—long after theinitial appearance of eukaryotes and long before a de-

finitive fossil record of metazoans, but in line with tracefossil evidence. The fossil record tells us that metazoanlife had its origin in the Proterozoic eon, at least 600million years ago, although trace fossils suggest thatthe earliest animals might have originated more than1.2 billion years ago.

The ancestors of both plants and animals were al-most certainly protists, suggesting that the phenomenonof multicellularity arose independently in the Metazoaand Metaphyta. Indeed, genetic and developmentaldata suggest that the basic mechanisms of pattern for-mation and cell–cell communication during develop-ment were independently derived in animals and inplants. In animals, segmental identity is established bythe spatially specific transcriptional activation of anoverlapping series of master regulatory genes, thehomeobox (Hox) genes. The master regulatory genes ofplants are not members of the homeobox gene family,but belong to the MADS box family of transcription fac-tor genes. There is no evidence that the animal home-obox and MADS box transcription factor genes are ho-mologous.

Although the fossil record is rich with the history ofmany early animal lineages, many others have left veryfew fossils. Many were very small, some were soft-bod-ied and did not fossilize well, and others lived whereconditions were not suitable for the formation of fossils.Therefore, we can only speculate about the abundanceof members of most animal groups in times past.However, groups such as the echinoderms (sea stars,urchins), molluscs (clams, snails), arthropods (crus-taceans, insects), corals, ectoprocts, brachiopods, andvertebrates have left rich fossil records. In fact, for somegroups (e.g., echinoderms, brachiopods, ectoprocts,molluscs), the number of extinct species known fromfossils exceeds the number of known living forms.Representatives of nearly all of the extant animal phylawere present early in the Paleozoic era, more than 500million years ago (mya). Life on land, however, did notappear until fairly recently, by geological standards, andterrestrial radiations began only about 470 mya.Apparently it was more challenging for life to invadeland than to first evolve on Earth! The following ac-count briefly summarizes the early history of life andthe rise of the invertebrates.

The Dawn of LifeIt used to be thought that the Proterozoic was a time of only a few simple kinds of life; hence the name.However, discoveries over the past 20 years haveshown that life on Earth began early and had a verylong history throughout the Proterozoic. It is estimatedthat Earth is about 4.6 billion years old, although theoldest rocks found are only about 3.8 billion years old.The oldest evidence of possible life on Earth consists of3.8-billion-year-old, debated, biogenic traces suspectedto represent anaerobic sulfate-reducing prokaryotes and

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‡Our great uncertainty about how many species of living organ-isms exist on Earth is unsettling and speaks to the issue of priori-ties and funding in biology. We know approximately how manygenes are in organisms from yeast (about 6,000 genes) to humans(about 10,000 genes), but taxonomic research has lagged behindother disciplines. At our current rate of species descriptions, itwould take us 2,000–8,000 years to describe the rest of Earth’s lifeforms. Not all of these new species are invertebrates—in fact, justbetween 1990 and 2002, 38 new primate species were discoveredand named. If prokaryotes are thrown into this mix, the numbersbecome even larger (one recent estimate suggested that a ton ofsoil could contain as many as 4 million species, or “different taxa,”of prokaryotes). However, at our current rate of anthropogenic-driven extinction, an estimated 90 percent of all species could goextinct before they are ever described. In the United States alone,at least 5,000 species are threatened with extinction, and an esti-mated 500 species have already gone extinct since people firstarrived in North America. Globally, the United NationsEnvironment Programme estimates that by 2030 nearly 25 percentof the world’s mammals could go extinct.§There are three popular theories on how life first evolved onEarth. The classic “primeval soup” theory, dating from StanleyMiller’s work in the 1950s, proposes that self-replicating organicmolecules first appeared in Earth’s early atmosphere and weredeposited by rainfall in the ocean, where they reacted further tomake nucleic acids, proteins, and other molecules of life. Morerecently, the idea of the first synthesis of biological molecules bychemical and thermal activity at deep-sea hydrothermal vents hasbeen suggested. The third proposal is that organic molecules firstarrived on Earth from another planet, or from deep space, oncomets or meteorites.


perhaps cyanobacterial stromatolites. The first certaintraces of prokaryotic life (secondary chemical evidenceof Cyanobacteria) occur in rocks dated at 2.5 billionyears, although fossil molecular residues of Cyano-bacteria have been found in rocks 2.7 billion years old.The first actual fossil traces of eukaryotic life (benthicalgae) are 1.7 to 2 billion years old, whereas the first cer-tain eukaryotic fossils (phytoplankton) are 1.4 to 1.7 bil-lion years old. Together, these bacteria and protists ap-pear to have formed diverse communities in shallowmarine habitats during the Proterozoic eon. Living stro-matolites (compact layered colonies of Cyanobacteriaand mud) are still with us, and can be found incertainhigh evaporation/high-salinity environments in suchplaces as Shark Bay (Western Australia), Scammon’sLagoon (Baja California), the Persian Gulf, the Paracascoast of Peru, the Bahamas, and Antarctica.

The Ediacaran Epoch and the Origin of AnimalsOne of the most perplexing unsolved mysteries in biol-ogy is the origin and early radiation of the Metazoa. Wenow know that by 600 mya, at the beginning of a periodin the late Proterozoic known as the Ediacaran epoch, aworldwide marine invertebrate fauna had alreadymade its appearance. If any animals existed before thistime, they left no known unambiguous fossil record.The Ediacaran fauna (600–570 mya) contains the firstevidence of many modern phyla, although the preciseevolutionary relationships of many of these fossils arestill being debated.* The modern phyla thought to be represented among the Ediacaran fauna includePorifera, Cnidaria, Echiura, Mollusca, Onychophora,Echinodermata, a variety of annelid-like forms (includ-ing possible pogonophorans), and quite probablyarthropods (soft-bodied trilobite-like organisms, anom-alocarids and their kin, etc.). However, many Ediacarananimals cannot be unambiguously assigned to any liv-ing taxa, and these animals may represent phyla orother high-level taxa that went extinct at the Protero-zoic–Cambrian transition.†

Ediacaran fossils were first reported from sites inNewfoundland and Namibia, but the name is derivedfrom the superb assemblages of these fossils discoveredat Ediacara in the Flinders Ranges of South Australia.Most of the Ediacaran organisms were preserved asshallow-water impressions on sandstone beds, but

some of the 30 or more worldwide sites represent deep-water and continental slope communities. The Edia-caran fauna was almost entirely soft-bodied, and therehave been no heavily shelled creatures reported fromthese deposits. Even the molluscs and arthropod-likecreatures from this fauna are thought to have had rela-tively soft (unmineralized, or lightly calcified) skeletons.A few chitinous structures developed during this time,such as the jaws of some annelid-like creatures (and thechitinous sabellid-like tubes of others) and the radulaeof early molluscs.‡ In addition, siliceous spicules ofhexactinellid sponges have been reported from Au-stralian and Chinese Ediacaran deposits. Many of theseProterozoic animals appear to have lacked complex in-ternal organ structures. Most were small and possessedradial symmetry. However, at least by late Ediacarantimes, large animals with bilateral symmetry had ap-peared, and some almost certainly had internal organs(e.g., the segmented, sheetlike Dickinsonia, whichreached a meter in length; Figure 1.2). The Ediacaranepoch was followed by the Cambrian period and thegreat “explosion” of skeletonized metazoan life associ-ated with that time (see below). Why skeletonized ani-mals appeared at that particular time, and in such greatprofusion, remains a mystery.

Geological evidence tells us that Earth’s earliest at-mosphere lacked free oxygen, and clearly the radiationof the animal kingdom could not have begun underthose conditions. Free oxygen probably accumulatedover many millions of years as a by-product of photo-synthetic activity in the oceans, particularly by theCyanobacterial (blue-green algae) stromatolites. How-ever, the evidence on free oxygen levels in theProterozoic is still a little murky. Significant atmospher-ic O2 levels may have been achieved fairly early in theProterozoic, 1.5 to 2.8 billion years ago, or perhaps evenearlier. Proterozoic seas might have been oxic near thesurface, but anoxic in deep waters and on the bottom.Some workers suggest that the absence of metazoan lifein the early fossil record is due to the simple fact that thefirst animals were small, lacked skeletons, and did notfossilize well, not to the absence of oxygen. The discov-ery of highly diverse communities of metazoan meio-fauna§ in the Proterozoic strata of south China and indeposits from the Middle and Upper Cambrian (e.g.,

INTRODUCTION 5

*During the 1980s, some workers believed that most of theEdiacaran biota was unrelated to modern phyla—that it was a“failed experiment” in the evolution of life on Earth. There waseven the suggestion that Ediacaran organisms be referred to a newphylum or even a new kingdom, the “Vendozoa,” which was saidto contain “quilted” organisms that lacked mouths and guts andpresumably received energy by absorbing dissolved organic mole-cules or by harboring photosynthetic or chemosynthetic sym-bionts. Today we know that this biota (now sometimes called the“Vendobionta”) actually represents only a portion of the Edia-caran biota, and the entire fauna includes many species nowviewed as primitive members of extant phyla.

†The largest mass extinctions occurred at the ends of the Protero-zoic era (Ediacaran epoch) and the Ordovician, Devonian, andPermian periods, and in the Early Triassic, Late Triassic, and end-Cretaceous. Most of these extinction events were experienced byboth marine and terrestrial organisms. An excellent review ofEdiacaran/Cambrian animal life can be found in Lipps and Signor(1992).‡Chitin is a cellulose-like family of compounds that is widely dis-tributed in nature, especially in invertebrates, fungi, and yeasts, butit is apparently uncommon in deuterostome animals and higherplants, perhaps due to the absence of the chitin synthase enzyme.§Meiofauna is usually defined as the interstitial animals that passthrough a 1 mm mesh sieve, but are retained by a 0.1 mm meshsieve.


the Swedish Orsten fauna) lends support to the ideathat many of the first animals were microscopic. Inthinking about the earliest metazoans, it is not difficultto imagine a microscopic primordial animal resemblinga colony of choanoflagellate protists whose cell–cell con-nections were enhanced by metazoan cell junctions andwhose inner and outer cells became separated and spe-cialized. However, large animals are not uncommonamong the Ediacaran and early Cambrian faunas.

It has also been proposed that the advent of predato-ry lifestyles was the key that favored the first appear-ance of animal skeletons (as defensive structures), lead-ing to the “Cambrian explosion.” The rapid appearanceand spread of diverse metazoan skeletons in the early

Cambrian heralded the beginning of the Phanerozoiceon. The Ediacaran fauna seems to have included pri-marily passive suspension and detritus feeders; veryfew of these animals appear to have been active carni-vores or herbivores. Only a few Ediacaran species areknown to have spanned the transition to the Cambrianperiod. Early Cambrian animal communities, on theother hand, included most of the trophic roles found inmodern marine communities, including giant predatoryarthropods.

The Paleozoic Era (570–250 mya)The Phanerozoic eon was ushered in with the almost si-multaneous appearance in the Lower Cambrian of well-developed calcareous body skeletons in numerousgroups, including archaeocyathans, molluscs, ecto-procts, brachiopods, crustaceans, and trilobites. The ap-pearance of mineralized animal skeletons thus definesthe beginning of the Cambrian, and it was an event offundamental importance in the history of life. Thenewly skeletonized animals radiated quickly and filleda multitude of roles in all shallow-water marine envi-ronments. The other major event at the Protero-zoic–Cambrian transition was the explosion of bilateral-ly symmetrical animals. Most of our modern metazoanphyla and classes were established as distinct lineages atthis time.

Much of what we know about early Cambrian lifecomes from the Lower Cambrian Chengjiang fossil de-posits of the Yunnan Province of southern China andsimilarly aged (although less well preserved) depositsspread across China and the Siberian Platform. The

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Figure 1.2 Some Ediacaran (late Proterozoic) animals.(A) Charnia and Charniodiscus, two Cnidaria resemblingmodern sea pens (Anthozoa, Pennatulacea). (B) A bushlikefossil of uncertain affinity (suggestive of a cnidarian). (C)Ediacara, a cnidarian medusa. (D) Dickinsonia, probably apolychaete annelid. (E) One of the numerous soft-bodiedtrilobites known from the Ediacaran period (some of whichalso occurred in the Early Cambrian).


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Chengjiang deposits are the oldest Cambrian occur-rences of well-preserved soft-bodied and hard-bodiedanimals, and they include a rich assemblage of exquis-itely preserved arthropods, onychophorans, medusae(Cnidaria), and brachiopods, many of which appearclosely related to Proterozoic Ediacaran species.

In the Middle Cambrian (e.g., the Burgess Shalefauna of western Canada and similar deposits else-where; Figure 1.3) polychaetes and tardigrades madetheir first positive appearances in the fossil record, andthe first complete echinoderm skeletons appeared. Inthe Upper Cambrian (e.g., the Orsten deposits of south-ern Sweden and similar strata), the first pentastomidCrustacea and the first agnathan fishes made their ap-pearances. By the end of the Cambrian, nearly all of themajor animal phyla had appeared.

The early Paleozoic also saw the first xiphosurans,eurypterids, trees, and teleost fishes (in the Ordovician).The first land animals (arachnids, centipedes, myri-apods) appeared in the Upper Silurian. By the middlePaleozoic (the Devonian), life on land had begun to pro-liferate. Forest ecosystems became established andbegan reducing atmospheric CO2 levels (eventually ter-minating an earlier Paleozoic greenhouse environment).The first insects also appeared in the middle Paleozoicfossil record. Insects developed flight in the LowerCarboniferous, and they began their long history of co-evolution with plants shortly thereafter (at least by themid-Carboniferous, when tree fern galls first appearedin the fossil record). During the Carboniferous period,global climates were generally warm and humid, andextensive coal-producing swamps existed.

The late Paleozoic experienced the formation of theworld supercontinent Pangaea in the Permian period(about 270 mya). The end of the Permian (250 mya) wasbrought about by the largest mass extinction known, inwhich 85 percent of Earth’s marine species (and 70 per-cent of the terrestrial vertebrate genera) were lost over abrief span of a few million years. The Paleozoic reefcorals (Rugosa and Tabulata) went extinct, as did theonce dominant trilobites, never to be seen again. The dri-ving force of the Permian extinction is thought to havebeen a huge asteroid impact, probably coupled withmassive Earth volcanism, and perhaps degassing ofstagnant ocean basins. The volcanism may have been thesame event that created the massive flood basalts knownas the Siberian Traps in Asia. This event may have led toatmospheric “pollution” in the form of dust and sulfurparticles that cooled Earth’s surface or massive gas emis-sions that led to a prolonged greenhouse warming.

The Mesozoic Era (250–65 mya)The Mesozoic era is divided into three broad periods:the Triassic, Jurassic, and Cretaceous. The Triassic beganwith the continents joined together as Pangaea. Theland was high, and few shallow seas existed. Global cli-mates were warm, and deserts were extensive. The ter-

restrial flora was dominated by gymnosperms, with an-giosperms first appearing in the latest part of the period.The oldest evidence of a flowering plant is from 130mya. Vertebrate diversity exploded in the Triassic. Onland, the first mammals appeared, as well as the turtles,pterosaurs, plesiosaurs, and dinosaurs. In Triassic seas,the diversity of predatory invertebrates and fishes in-creased dramatically, although the paleogeological datasuggest that deeper marine waters might have been toolow in oxygen to harbor much (or any) multicellular life.The end of the Triassic witnessed a sizable global extinc-tion event, perhaps driven by the combination of aster-oid impact and widespread volcanism that created theCentral Atlantic Magmatic Province of northeasternSouth America 200 mya.

The Jurassic saw a continuation of warm, stable cli-mates, with little latitudinal or seasonal variation andprobably little mixing between shallow and deep ocean-ic waters. Pangaea split into two large land masses, thenorthern Laurasia and southern Gondwana, separatedby a circumglobal tropical seaway known as the TethysSea. Many tropical marine families and genera today arethought to be direct descendants of inhabitants of thepantropical Tethys Sea. On land, modern genera ofmany gymnosperms and advanced angiosperms ap-peared, and birds began their dramatic radiation. Leaf-mining insects (lepidopterans) appeared by the lateJurassic (150 mya), and other leaf-mining orders ap-peared through the Cretaceous, coincident with the ra-diation of the vascular plants.

In the Cretaceous, large-scale fragmentation of Gond-wana and Laurasia took place, resulting in the forma-tion of the Atlantic and Southern Oceans. During thisperiod, land masses subsided and sea levels were high;the oceans sent their waters far inland, and great epi-continental seas and coastal swamps developed. Asland masses fragmented and new oceans formed, glob-al climates began to cool and oceanic mixing began tomove oxygenated waters to greater depths in the sea.The end of the Cretaceous was marked by the Cre-taceous–Tertiary mass extinction, in which an estimated50 percent of Earth’s species were lost, including the di-nosaurs and all of the sea’s rich Mesozoic ammonite di-versity. There is strong evidence that this extinctionevent was driven by a combination of two factors: amajor asteroid impact (probably in the Yucatan region ofmodern Mexico) and massive Earth volcanism associat-ed with the great flood basalts of India known as theDeccan Traps.

The Cenozoic Era (65 mya–present)The Cenozoic era dawned with a continuing worldwidecooling trend. As South America decoupled fromAntarctica, the Drake Passage opened to initiate the cir-cum-Antarctic current, which eventually drove the for-mation of the Antarctic ice cap, which in turn led to ourmodern cold ocean bottom conditions (in the Miocene).

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Figure 1.3 Some Cambrian life forms from the BurgessShale deposits of Canada. (A) Canadaspis, an early mala-costracan crustacean. (B) Yohoia, an arthropod of uncer-tain classification. (C) Two species of Anomalocaris, A.nathorsti (above) and A. canadensis. Anomalocarids wereonce thought to represent an extinct phylum of segment-ed animals, but are now regarded by many workers asprimitive crustaceans dating back to the Ediacaran. (D) Wiwaxia, a Burgess Shale animal with no clear affinityto any known metazoan phylum (although some workersregard it as a polychaete annelid). (E) Nectocaris, anothercreature that has yet to be classified into any known phy-

lum (despite its strong chordate-like appearance). (F) Dinomischus, a stalked creature with a U-shaped gutand with the mouth and anus both placed on a radiallysymmetrical calyx. Although superficially resembling sever-al extant phyla, Dinomischus is now thought to belong toan unnamed extinct phylum of sessile Cambrian animals.(G) The elusive Odontogriphus, an appendageless flattenedvermiform creature of unknown affinity. (H) One of themore enigmatic of the Burgess Shale animals, Opabinia;this segmented creature was probably an ancestral arthro-pod. Notice the presence of five eyes, a long prehensile“nozzle,” and gills positioned dorsal to lateral flaps.

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India moved north from Antarctica and collided withsouthern Asia (in the early Oligocene). Africa collidedwith western Asia (late Oligocene/early Miocene), sep-arating the Mediterranean Sea from the Indian Oceanand breaking up the circumtropical Tethys Sea.Relatively recently (in the Pliocene), the Arctic ice capformed, and the Panama isthmus rose, separating theCaribbean Sea from the Pacific and breaking up the lastremnant of the ancient Tethys Sea about 3.5 mya.Modern coral reefs (scleractinian-based reefs) appearedearly in the Cenozoic, reestablishing the niche once heldby the rugose and tabulate corals of the Paleozoic.

This textbook focuses primarily on invertebrate life atthe very end of the Cenozoic, in the Recent (Holocene)epoch. However, evaluation of the present-day “suc-cess” of animal groups also involves consideration ofthe history of modern lineages, the diversity of life overtime (numbers of species and higher taxa), and theabundance of life (numbers of individuals). The pre-dominance of certain kinds of invertebrates today is un-questionable. For example, of the 1,291,364 or so de-scribed species of animals (1,244,694 of which areinvertebrates), 85 percent are arthropods. Most arthro-pods today are insects, probably the most successfulgroup of animals on Earth. But the fossil record tells usthat arthropods have always been key players in thebiosphere, even before the appearance of the insects.Box 1B conveys a general idea of the levels of diversityamong the animal phyla today.

Where Do Invertebrates Live?Marine HabitatsEarth is a marine planet—salt water covers 71 percent ofits surface. The vast three-dimensional world of the seascontains 99 percent of Earth’s inhabited space. Life al-most certainly evolved in the sea, and the major eventsdescribed above leading to the diversification of inverte-brates occurred in late Proterozoic and early Cambrianshallow seas. Many aspects of the marine world mini-mize physical and chemical stresses on organisms. Thebarriers to evolving gas exchange and osmotic regulato-ry structures that can function in freshwater and terres-trial environments are formidable, and relatively fewlineages have escaped their marine origins to do so.Thus, is not surprising to find that the marine environ-ment continues to harbor the greatest diversity of high-er taxa and major body plans. Some phyla (e.g., echino-derms, sipunculans, chaetognaths, cycliophorans,placozoans, echiurans, ctenophores) have remained ex-clusively marine. Productivity in the world’s oceans isvery high, and this also probably contributes to the highdiversity of animal life in the sea (the total primary pro-ductivity of the seas is about 48.7 × 109 metric tons ofcarbon per year). Perhaps the most significant factor,however, is the special nature of seawater itself.

Water is a very efficient thermal buffer. Because of itshigh heat capacity, it is slow to heat up or cool down.

INTRODUCTION 9

Specialists in certain groups estimate that the known kinds of organisms probably represent only a small fraction of actualexisting species. Note that we have broken down the phyla Arthropoda and Chordata into their respective subphyla, andthat we have lumped the protist phyla together (see Chapter 5 for a complete classification of the protists). Of the1,297,708 estimated described species of Animalia (excluding protists), 1,251,038 (96 percent) are invertebrates.

BOX 1B Approximate Numbers of Known Extant Species in Various Groups

Kingdom Protista (80,000)

Porifera (5,500)

Cnidaria (10,000)

Ctenophora (100)

Placozoa (1)

Monoblastozoa (1)

Rhombozoa (70)

Orthonectida (20)

Platyhelminthes (20,000)

Nemertea (900)

Gnathostomulida (80)

Rotifera (1,800)

Gastrotricha (450)

Kinorhyncha (150)

Nematoda (25,000)

Nematomorpha (230)

Priapula (16)

Acanthocephala (700)

Cycliophora (1)

Entoprocta (150)

Loricifera (10)

Annelida (16,500)

Echiura (135)

Sipuncula (320)

Tardigrada (600)

Onychophora (110)

Arthropoda (1,097,631)

Cheliceriformes (70,000)

Crustacea (68,171)

Hexapoda 948,000

(estimates range from

870,000 to 1,500,000)

Myriapoda (11,460)

Mollusca (50,000)

Brachiopoda (335)

Ectoprocta (4,500)

Phoronida (20)

Chaetognatha (100)

Echinodermata (7,000)

Hemichordata (85)

Chordata (49,693)

Urochordata (3,000)

Cephalochordata (23)

Vertebrata (46,670)


Large bodies of water, such as oceans, absorb and losegreat amounts of heat with little change in actual watertemperature. Oceanic temperatures are very stable incomparison with those of freshwater and terrestrial en-vironments. Short-term temperature extremes occuronly in intertidal and estuarine habitats; invertebratesliving in such areas must possess behavioral and physi-ological adaptations that allow them to survive thesetemperature changes, which are often combined withaerial exposure during low tide periods.

The saltiness, or salinity, of seawater averages about3.5 percent (usually expressed as parts per thousand,35‰). This property, too, is quite stable, especially inareas away from shore and the influence of freshwaterrunoff. The salinity of seawater gives it a high density,which enhances buoyancy, thereby minimizing energyexpenditures for flotation. Furthermore, the variousions that contribute to the total salinity occur in fairlyconstant proportions. These qualities result in a totalionic concentration in seawater that is similar to that inthe body fluids of most animals, minimizing the prob-lems of osmotic and ionic regulation (see Chapter 3).The pH of seawater is also quite stable throughout mostof the ocean. Naturally occurring carbonate compoundsparticipate in a series of chemical reactions that bufferseawater at about pH 7.5–8.5. However, today’s anthro-pogenic changes in atmospheric CO2 threaten to alterthe carbonate buffering capacity of the world’s seas.

In shallow and nearshore waters, carbon dioxide,various nutrients, and sunlight are generally availablein quantities sufficient to allow high levels of photosyn-thesis, either seasonally or continuously (depending onlatitude and other factors). Dissolved oxygen levels

rarely drop below those required for normal respiration,except in stagnant waters such as might occur in certainestuarine or ocean basin habitats, or where anthro-pogenic activities have created eutrophic conditions.

Because the marine realm is home to most of the ani-mals discussed in this book, some terms that describe thesubdivisions of that environment and the categories ofanimals that inhabit them will be useful. Figure 1.4 illus-trates a generalized cross section through an ocean. Theshoreline marks the littoral region, where sea, air, andland meet and interact (Figure 1.5A). Obviously, this re-gion is affected by the rise and fall of the tides, and wecan subdivide it into zones or shore elevations relative tothe tides. The supralittoral zone, or splash zone, is rarelycovered by water, even at high tide, but it is subjected tostorm surges and spray from waves. The eulittoral zone,or true intertidal zone, lies between the levels of the high-est and lowest tides. It can be subdivided by its flora andfauna, and by mean monthly hours of aerial exposure,into high, mid-, and low intertidal zones. The sublittoralzone, or subtidal zone, is never uncovered, even at verylow tides, but it is influenced by tidal action (e.g., bychanges in turbulence, turbidity, and light penetration).

Organisms that inhabit the world’s littoral regionsare subjected to dynamic and often demanding condi-

10 CHAPTER ONE

Figure 1.4 A schematic cross section of the major habi-tat regions of the ocean (not drawn to scale).


tions, and yet these areas commonly are home to excep-tionally high numbers of species. As noted above, mostanimals and plants are more or less restricted to particu-lar elevations along the shore, a condition resulting inthe phenomenon of zonation. Such zones are visible asdistinct bands or communities of organisms along theshoreline. The upper elevational limit of an intertidal or-ganism is commonly established by its ability to tolerate

INTRODUCTION 11

Figure 1.5 A few of Earth’s major habitat types. (A)Exposed rocks and algae in the intertidal zone, northernCalifornia. (B) A tidal flat and bordering salt marsh innorthern California. (C) A mangrove swamp at low tide, inMexico. (D) A freshwater stream in a tropical wet forest(“rain forest”), Costa Rica. (E) Flowering trees in a tropicaldry forest, Costa Rica. (F) The Sonoran desert.

(A)

(B)

(C)

(D)

(E) (F)

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conditions of exposure to air (e.g., desiccation, tempera-ture fluctuations), whereas its lower elevational limit isoften determined by biological factors (competitionwith or predation by other species). There are, of course,many exceptions to these generalizations.

Extending seaward from the shoreline is the conti-nental shelf, a feature of most large land masses. Thecontinental shelf may be only a few kilometers wide, orit may extend up to 1,000 km from shore (50 to 100 km isaverage for most areas). It usually reaches a depth of150–200 m. These nearshore shelf areas are among themost productive environments of the ocean, being richin nutrients and shallow enough to permit photosynthe-sis over much of the area.

The outer limit of the continental shelf—called thecontinental edge—is indicated by a relatively suddenincrease in the steepness of the bottom contour. The“steep” parts of the ocean floor, the continental slopes,actually have slopes of only 4–6 percent (although theslope is much steeper around volcanic islands). The con-tinental slope continues from the continental edge to thedeep ocean floor, which forms the expansive, relativelyflat abyssal plain. The abyssal plain lies an average ofabout 4 km below the sea’s surface, but it is interruptedby a variety of ridges, sea mounts, abyssal mountainranges, trenches, and other formations. The bottoms ofdeep-sea trenches can exceed 10 km in depth.

Organisms that inhabit the water column are knownas pelagic organisms, whereas those living on the seabottom anywhere along the entire contour shown inFigure 1.4 are referred to as benthic organisms. Both thevariety and the abundance of life tend to decrease withincreasing depth, from the rich littoral and continentalshelf environments to the deep abyssal plain. However,an overgeneralization of this relationship can be mis-leading. For example, although pelagic biomass de-clines exponentially with depth, both diversity and bio-mass increase again near the bottom, in a thick layer ofresuspended sediments called the benthic boundarylayer. Also, shelf and slope habitats in temperate re-gions are often characterized by low animal density buthigh species diversity. In many areas, benthic diversityincreases abruptly below the continental edge (100–300m depth), peaks at 1,000 to 2,000 m depth, and then de-creases gradually. Species diversity in the benthicabyssal region itself may be surprisingly high. The firstimpression of early marine scientists—that the deep seabed was an environment able to sustain only a fewspecies in impoverished simple communities—wassimply wrong.

Benthic animals may live on the surface of the sub-stratum (epifauna, or epibenthic forms, such as mostsea anemones, sponges, many snails, and barnacles) orburrow within soft substrata (infauna). Infaunal formsinclude many relatively large invertebrates, such asclams and various worms, as well as some specialized,very tiny forms that inhabit the spaces between sand

grains, termed interstitial organisms (the smallest ofwhich are meiofauna, animals smaller than 0.5 mm).Benthic animals may also be categorized by their loco-motor capabilities. Animals that are generally quitemotile and active are described as being errant (e.g.,crabs, many worms), whereas those that are firmly at-tached to the substratum are sessile (e.g., sponges,corals, barnacles). Others are unattached or weakly at-tached, but generally do not move around much(e.g.,crinoids, solitary anemones, most clams); these animalsare said to be sedentary.

The region of water extending from the surface tonear the bottom of the sea is called the pelagic zone. Thepelagic region over the continental shelf is called theneritic zone, and that over the continental slope and be-yond is called the oceanic zone. The pelagic region canalso be subdivided into increments on the basis of waterdepth (Figure 1.4) or the depth to which light pene-trates. The latter factor is, of course, of paramount bio-logical importance. Only within the photic zone doesenough sunlight penetrate that photosynthesis canoccur, and (except in a few special circumstances) all lifein the deeper, aphotic zone depends ultimately uponorganic input from the overlying sunlit layers of the sea.Notable exceptions are the restricted deep-sea hy-drothermal vent and benthic cold seep communities, inwhich sulfur-fixing microorganisms serve as the basis ofthe food chain.* The photic zone can be up to 200 mdeep in the clear waters of the open ocean, decreasing toabout 40 m over continental shelves and to as little as 15m in some coastal waters. Note that some oceanogra-phers restrict the term “aphotic zone” to depths below1,000 m, where absolutely no sunlight penetrates; the re-gion between this depth and the photic zone is thencalled the disphotic zone.

Organisms that inhabit the pelagic zone are often de-scribed in terms of their relative powers of locomotion.Pelagic animals that are strong swimmers, such as fish-es and squids, constitute the nekton. Those pelagicforms that simply float and drift, or generally are at themercy of water movements, are collectively called theplankton. Many planktonic animals (e.g., small crus-taceans) actually swim very well, but they are so smallthat they are swept along by prevailing currents in spiteof their swimming movements, even though thosemovements may serve to assist them in feeding or es-caping predators. Both plants (phytoplankton) and ani-mals (zooplankton) are included among the plankton,

12 CHAPTER ONE

*In addition to deep-sea hydrothermal vents, nonphotosyntheticchemoautotroph-based communities have recently been discov-ered in a cave (Movile Cave in Romania). The base of the foodchain in this unique ecosystem consists of autotrophic microor-ganisms (bacteria and fungi) thriving in thin mats in and neargeothermal waters that contain high levels of hydrogen sulfide.These communities, which sustain dozens of microbial and inver-tebrate species, create pockets of oxygen-poor, CO2- and methane-rich air. It is thought that the hydrogen sulfide originates from adeep magmatic source, similar to that seen in deep-sea vents.


the latter being represented by invertebrates such as jel-lyfishes, comb jellies, arrow worms, many small crus-taceans, and the pelagic larvae of many benthic adults.Planktonic animals that spend their entire lives in thepelagic realm are called holoplanktonic animals; thosewhose adult stage is benthic are called meroplanktonicanimals.

Estuaries and Coastal MarshlandsEstuaries usually occur along low-lying coasts and arecreated by the interaction of fresh and marine waters,typically where rivers enter the sea. Here one finds anunstable blending of freshwater and saltwater condi-tions, moving water, tidal influences, and drastic sea-sonal changes. Estuaries receive high concentrations ofnutrients from terrestrial runoff in their freshwatersources and are typically highly productive environ-ments. Temperature and salinity vary greatly with tidalactivity and with season. Depending on tides and tur-bulence, the waters of estuaries may be relatively wellmixed and more or less homogeneously brackish, orthey may be distinctly stratified, with fresh water float-ing on the denser salt water below.

The amount of dissolved oxygen in an estuary mayalso change markedly throughout a 24-hour cycle as afunction of temperature and the metabolism of au-totrophs. In many cases, hypoxic conditions may occuron a daily basis, especially in the early morning hours.Animals inhabiting these areas must be capable of mi-grating to regions of higher oxygen levels, be able tostore oxygen bound to certain body fluid pigments, orbe able to switch temporarily to metabolic processesthat do not require oxygen-based respiration. Further-more, vast amounts of silt borne by freshwater runoffare carried into the waters of estuaries; most of this siltsettles out and creates extensive tidal flats (Figure 1.5B).In addition to the natural stresses common to estuarineexistence, the inhabitants of estuaries are also subject tostresses resulting from human activity—pollution, ther-mal additions from power plants, dredging and filling,excessive siltation resulting from coastal and upland de-forestation and development, and storm drain dis-charges are some examples.

Most coastal swamps and marshlands, such as saltmarshes and mangrove swamps, are characterized bystands of halophytes (flowering plants that flourish insaline conditions; Figure 1.5B,C). Salt marshes and man-grove swamps are alternately flooded and uncovered bytidal action within the estuary, and are thus subjected tothe fluctuating conditions described above. The densehalophyte stands and the mixing of waters of differentsalinities create an efficient nutrient trap. Instead ofbeing swept out to sea, most dissolved nutrients enteringan estuary (or generated within it) are utilized there,yielding some of the most productive regions in theworld. This great productivity does eventually enter thesea in two principal ways: as plant detritus (mainly from

halophyte debris), and via the nektonic animals that mi-grate in and out of the estuary. The contribution of estu-aries to general coastal productivity can hardly be exag-gerated. The organic matter produced by plants of theFlorida Everglades, for example, forms the base of amajor detritus food web that culminates in the rich fish-eries of Florida Bay. Furthermore, an estimated 60–80percent of the world’s commercial marine fishes rely onestuaries directly, either as homes for migrating adults oras protective nurseries for the young. Estuaries and othercoastal wetlands are also of prime importance to bothresident and migratory populations of water birds.

A large number of invertebrates have adapted to lifein these dynamic environments. In general, animalshave but two alternatives when encountering stressfulconditions: either they migrate to more favorable envi-ronments, or they remain and tolerate (accommodateto) the changing conditions. Many animals migrate intoestuaries to spend only a portion of their life cycle,whereas others move in and out on a daily basis withthe tides. Other species remain in estuaries throughouttheir lives, and these species show a remarkable rangeof physiological adaptations to the environmental con-ditions with which they must cope (Chapter 3).

Freshwater HabitatsBecause bodies of fresh water are so much smaller thanthe oceans, they are much more readily and drasticallyinfluenced by extrinsic environmental factors, and thusare relatively unstable environments (Figure 1.5D).Changes in temperature and other conditions in ponds,streams, and lakes may occur quickly and be of a mag-nitude never experienced in most marine environments.Seasonal changes are even more extreme, and may in-clude complete freezing during the winter and com-plete drying in the summer. Ponds that hold water foronly a few weeks during and after rainy seasons arecalled ephemeral pools (or vernal pools). They typicallycontain a unique and highly specialized invertebratefauna capable of producing resting, or diapause, stages(usually eggs or embryos) that can survive for monthsor even years without water. As stressful as this sounds,ephemeral pools contain rich communities of plant andanimal life, especially endemic species of crustaceans(e.g., King et al. 1996). Diapause is a form of dormancyin which invertebrates in any stage of development be-fore the adult, including the egg stage, cease theirgrowth and development. Diapause is genetically deter-mined. Some species are programmed to enter diapausewhen certain environmental conditions provide theproper cues (often a combination of temperature andlength of daylight). Hibernation and aestivation aretwo other types of dormancy, but they are not genetical-ly programmed and may occur irregularly, or not at all,during any stage of an animal’s development. Hiber-nation is a temporary response to cold, while aestivationis a temporary response to heat.


The very low salinity of fresh water (rarely more than1‰) and the lack of constant relative ion concentrationssubject freshwater inhabitants to severe ionic and os-motic stresses. These conditions, along with other fac-tors such as reduced buoyancy, less stable pH, andrapid nutrient input and depletion produce environ-ments that support far less biological diversity than theocean does. Nonetheless, many different invertebratesdo live in fresh water and have solved the problems as-sociated with this environment. Special adaptations tolife in fresh water are summarized in Chapter 3 and dis-cussed in relation to the groups of invertebrates thathave such adapations in later chapters.*

Terrestrial HabitatsLife on land is in many ways even more rigorous thanlife in fresh water. Temperature extremes are usually en-countered on a daily basis, water balance is a criticalproblem, and just physically supporting the body re-quires major expenditures of energy. Water provides amedium for support, for dispersing gametes, larvae, andadults, and for diluting waste products, and is a sourceof dissolved materials needed by animals. Animals liv-ing in terrestrial environments do not enjoy these bene-fits of water, and must pay the price. Adaptations to ter-restrial living are discussed in Chapter 3.

Relatively few higher taxa have successfully invadedthe terrestrial world. Invertebrate success on land is ex-emplified by the arthropods, notably the terrestrialisopods, insects, spiders, mites, scorpions, and otherarachnids. These arthropod groups include truly terres-trial species that have invaded even the most arid envi-ronments (Figure 1.5F). Except for some snails and nema-todes, all other land-dwelling invertebrates, includingsuch familiar animals as earthworms, are largely restrict-ed to relatively moist areas. In a very real sense, manysmaller terrestrial invertebrates survive only through thepermanent or periodic presence of water.

A Special Type of Environment: SymbiosisMany invertebrates live in intimate association withother animals or plants. This kind of association istermed a symbiotic relationship, or simply symbiosis.Symbiosis was first defined in 1879 by German mycolo-gist H. A. DeBary as “unlike organisms living together.”In most symbiotic relationships, a larger organism(called the host) provides an environment (its body, bur-row, nest, etc.) on or within which a smaller organism(the symbiont) lives. Some symbiotic relationships arerather transient—for example, the relationship between

ticks or lice and their vertebrate host—whereas othersare more or less permanent. Some symbionts are oppor-tunistic (facultative), whereas others cannot survivewithout their host (obligatory).

Symbiotic relationships can be subdivided into sever-al categories based on the nature of the interaction be-tween the symbiont and its host. Perhaps the most fa-miliar type of symbiotic relationship is parasitism, inwhich the symbiont (a parasite) receives benefits at thehost’s expense. Parasites may be external (ectopara-sites), such as lice, ticks, and leeches; or internal (en-doparasites), such as liver flukes, some roundworms,and tapeworms. Other parasites may be neither strictlyinternal nor strictly external; rather, they may live in abody cavity or area of the host that communicates withthe environment, such as the gill chamber of a fish orthe mouth or anus of a host animal (mesoparasites).Some parasites live their entire adult lives in associationwith their hosts and are permanent parasites, whereastemporary, or intermittent parasites, such as bedbugs,only feed on the host and then leave it. Parasites thatparasitize other parasites are hyperparasitic. Temporaryparasites, such as mosquitoes and aegiid isopods, areoften referred to as micropredators, in recognition of thefact that they usually “prey” on several different host in-dividuals. Parasitoids are insects, usually flies or wasps,whose immature stages feed on their hosts’ bodies, usu-ally other insects, and ultimately kill the host. A defini-tive host is one in which the parasite reaches reproduc-tive maturity. An intermediate host is one that isrequired for parasite’s development, but in which theparasite does not reach reproductive maturity.

A few groups of invertebrates are predominantly orexclusively parasitic, and almost all invertebrate phylahave at least some species that have adopted parasiticlifestyles. Many texts and courses on parasitology payparticular attention to the effects of these animals on hu-mans, crops, livestock, and economic conditions. Herewe also try to focus on parasitism from “the parasite’spoint of view,” that is, as a particular lifestyle suited to aspecific environment, requiring certain adaptations andconferring certain advantages. It has been estimatedthat 50 to 70 percent of the world’s species are parasitic,making parasitism the most common way of life. Sinceinsects are the most diverse group of organisms onEarth, and since all insects harbor numerous parasites, itis fair to say that the most common mode of life onEarth is that of an insect parasite.

Mutualism is another form of symbiosis that is gener-ally defined as an association in which both host and sym-biont benefit. Such relationships may be extremely inti-mate and important for the survival of both parties; forexample, the bacteria in our own large intestine are im-portant in the production of certain vitamins and in pro-cessing material in the gut. In fact, beneficial associationswith specific bacterial symbionts characterize many, if notall, animal species, although most of these relationships

14 CHAPTER ONE

*Freshwater habitats are some of the most threatened environ-ments on Earth. Throughout the United States, people destroy100,000 acres of wetlands annually. Rare aquatic habitats such asephemeral pools and subterranean rivers are disappearing fasterthan they can be studied. Underground, or hypogean, habitats areoften aquatic, and these habitats are quickly being destroyed bypollution and groundwater overdraft.


have not been studied. Another example is the relation-ship between termites and certain protists that inhabittheir digestive tracts and are responsible for the break-down of cellulose into compounds that can be assimilatedby their insect hosts. Other mutualistic relationships maybe less binding on the organisms involved. Cleanershrimps, for example, inhabit coral reef environments,where they establish “cleaning stations” that are visitedregularly by reef-dwelling fishes that present themselvesto the shrimps for the removal of parasites. Obviously,even this rather loose association results in benefits for theshrimps (a meal) as well as for the fishes (removal of para-sites). The mutualistic relationships between plants andtheir pollinators are essential to the survival of most flow-ering plants and their insect partners (and, in some cases,their bird or nectar-feeding bat partners).

A third type of symbiosis is called commensalism.This category is something of a catch-all for associationsin which significant harm or mutual benefit is not obvi-ous. Commensalism is usually described as an associa-tion that is advantageous to one party (the symbiont) butleaves the other (the host) unaffected. For instance,among invertebrates there are numerous examples ofone species inhabiting the tube or burrow of another (in-quilism); the former obtains protection, food, or bothwith little or no apparent effect on the latter. A specialtype of commensalism is phoresis, wherein the twosymbionts “travel together,” but there is no physiologicalor biochemical dependency on the part of either partici-pant. Usually one phoront is smaller than the other andis mechanically carried about by its larger companion.

There is a good deal of overlap among the categoriesof symbiosis described above, and many animal rela-tionships have elements of two or even of all the cate-gories, depending on life history stage or environmentalconditions. Taken in its broad sense, the concept of sym-biosis has profound implications for understandingEarth’s biodiversity. It has been said that at least half theplanet’s species are symbionts and that all species havesymbiotic partnerships—concepts suggesting that everyindividual is an ecosystem.

Some Comments On EvolutionFitness By Any Other Name Would Be As Loose

A group ineptMight better optTo be adeptAnd so adoptWays more aptTo wit, adapt.

John BurnsBiograffiti, 1975

This book takes evolution as its central theme. However,the paradigms that have guided evolutionary biology

for the past 60 years are presently in the midst of a majorreevaluation. This reevaluation has been precipitated bythree phenomena. First is the revolution in molecular bi-ology, which has produced dramatic discoveries sincethe late 1970s and will no doubt continue to do so formany decades to come. Second is the continuing devel-opment of an explicit method of inferring phylogenies,called phylogenetic systematics or cladistics (seeChapter 2). Third is the development of some very newand different ideas regarding the operation of evolutionitself. Most students are familiar with Darwin’s theoryof natural selection, and with the fundamental geneticmechanisms that underlie adaptation, but fewer stu-dents are familiar with more recent ideas that have beenproposed outside the framework of natural selectionand adaptation. We briefly review some of these inter-esting new thoughts, all of which have implications forthe processes represented by the phylogenetic trees ap-pearing in the following chapters.

There are three fundamental patterns we see when weexamine evolutionary history: anagenesis, speciation,and extinction. Anagenesis seems to be driven by thoseneo-Darwinian processes often referred to as microevo-lution—the within-species, generation-by-generationevolution of populations and groups of populations overthe “lifetime” of a species. Natural selection and adapta-tion are powerful driving forces at this level. Speciationis the “birth” of a species, and extinction is the “death”(termination) of a species. Speciation and extinction en-gage processes outside the natural selection–adaptationparadigm—processes often referred to as macroevolu-tion. The mechanisms that initiate and sculpt each ofthese patterns differ. Most college courses today focusprimarily on microevolution, or anagenesis, and moststudents reading this book already know a great dealabout population genetics and natural selection.However, the view that all of evolution can be under-stood solely on the basis of microevolutionary phenome-na is being reexamined in light of new ideas regardingevolutionary change. Consequently, we would like to in-troduce readers to some ideas with which they might beless familiar. We will do so by first discussing within-species processes (presented here under the term “mi-croevolution”), and then speciation and extinction(grouped under the heading “macroevolution”).

MicroevolutionThe neo-Darwinian evolutionary model, or so-calledmodern synthesis, that resulted from the integration ofMendelian genetics into Darwinian natural selectiontheory dominated evolutionary biology through thetwentieth century. Basically, the neo-Darwinian viewholds that all evolutionary changes result from the ac-tion of natural selection on variation within populations(see John Burns’s poem above). This view has beencalled the “adaptationist paradigm.” The theory focuseson adaptation and deals primarily with genes and


changes in allelic frequencies within populations. Thesegenetic variations come about primarily by recombina-tion and mutation, although the random phenomena ofgenetic drift and the founder effect are also part of theneo-Darwinian synthesis.

Evolution by natural selection is viewed as a deter-ministic process, even though certain elements ofchance are accepted within the theory (e.g., mutation,random mating, the founder effect). The theory of nat-ural selection implies that, given a complete under-standing of the environment and genetics, evolutionaryoutcomes should be largely predictable. The theory ofnatural selection further implies that virtually all of thecharacteristics animals possess are products of adapta-tions leading to increased fitness (ultimately, to in-creased reproductive success). An adaptationist viewmight lead one to assume that every aspect of an ani-mal’s phenotype is the product of natural selectionworking to increase the fitness of a species in a particu-lar environment.

Microevolution is thus seen to be a deterministic,within-species phenomenon that affects population ge-netics on a generation-to-generation basis to producechanges and patterns in gene frequencies within andamong populations. The modern synthesis deals almostexclusively with evolution at this level.

MacroevolutionMacroevolution is the focus of some of the most inter-esting debates among evolutionists today. Macroevo-lutionary phenomena include such things as the originof species and radiations of species lineages (cladogene-sis), “explosive” radiations that appear to be linked tothe opening up of new ecological arenas or niches,transgenic events, major shifts in developmental proc-esses that might result in new body plans, various kary-otypic alterations (e.g., polyploidy and polyteny), geo-logical events that profoundly alter the distributions ofspecies, and mass extinctions (and the subsequent newbiotic proliferations).

Mass extinction events in Earth’s history have playedmajor roles in reshaping the directions of animal evolu-tion in unpredictable ways. The largest of these extinc-tion events wiped out a majority of life forms on Earth.In the Permian–Triassic event described above, for ex-ample, an estimated 85 percent of all marine specieswent extinct (although no phylum is known to havegone extinct since the start of the Cambrian). Mass ex-tinctions thus are profound macroevolutionary eventsthat can abruptly (in geological time) terminate millionsof species and lineages.

In contrast to microevolution, macroevolution is evo-lutionary change, often rapid, that produces phyloge-netic patterns formation above the species level (e.g., thepatterns depicted on the phylogenetic trees in thisbook). The fossil record suggests that speciation events(one species giving rise to one or more new species)

tend to be rapid, or geologically instantaneous. Analysisof the fossil record also shows that the number ofspecies has increased, perhaps exponentially, since theend of the Proterozoic, with this diversification periodi-cally interrupted by mass extinctions. And mass extinc-tions have always been followed by periods of rapidspeciation and radiation at higher taxonomic levels (i.e.,macroevolution).

Newer views suggest that speciation might not beinitiated by natural selection, but rather by processesoutside the natural selection paradigm—most frequent-ly by purely stochastic processes. Microevolution can bethought of as a within-species process that maintains ge-nomic continuity and continually “fine-tunes” popula-tions and species to their changing environment. A rea-sonable analogy might be the basic metabolic activitiesthat keep your own body “fine-tuned” to the environ-ment—a background process that is always at workmaintaining a level of homeostasis (within your body,or within a species’ gene pool). A macroevolutionaryevent, on the other hand, is typically a processes that dis-rupts genomic, or reproductive, continuity in a speciesand may thus initiate speciation events. Following theabove analogy, macroevolutionary events disrupt thehomeostasis of species’ gene pools.

One of the most fundamental new approaches toevolutionary biology is the consideration of stochasticprocesses or events—those that occur at random or bychance. Some examples of stochastic events are de-scribed below.

The geneticist Goldschmidt, the paleontologistSchindewolf, and the zoologists Jeannel, Cuénot, andCannon all maintained until the 1950s that neither evo-lution within species nor simple allopatric speciationcould fully explain macroevolution. They advanced anidea called saltation theory—the sudden origin ofwholly new types of organisms—the “hopeful mon-sters” of Goldschmidt—in great leaps of change. It hasbeen proposed that one way such rapid changes mightoccur is through transgenic events, involving the “later-al transfer” of genetic material from one species to an-other. Two mechanisms of lateral genetic transfer havebeen implicated as possible agents of saltation: trans-posable genetic elements and symbiogenesis.

Transposable elements (TEs) are specialized DNAsegments that move (transpose) from one location to an-other, either within a cell’s DNA, between individuals ina species, or even between species. They were discov-ered in maize (Zea mays) by the Nobel laureate BarbaraMcClintock in the 1950s, but little was known aboutthem until recently. With the growth of molecular genet-ics, hundreds of TEs now have been identified—over 40different ones are known from the laboratory fruit flyDrosophila melanogaster alone. The mechanisms of TEtransfer between organisms are not yet well under-stood. However, the transfer of genetic elements fromone species to another is suspected to be by way of

16 CHAPTER ONE UNCORRECTED PAGE PROOFS

viruses, bacteria, arthropod parasites, or other vectors.There is strong evidence that parasitic mites have beenresponsible for the lateral transfer of genetic elementsamong Drosophila species.

The movement of a TE within a genome is mediatedby a TE-encoded protein called a transposase, probablyinteracting in complex ways with certain cellular fac-tors. A transposase recognizes the ends of the TE, breaksthe DNA at these ends to release the TE from its originalposition, and joins the ends to a new target sequence.The transposition of some TEs from bacteria to bacteria,and from bacteria to plant cells, is partially understood,and we know that the introduction of these DNA seg-ments can contribute powerful mutagenic qualities tothe new host’s genome. Recent work suggests that agreat deal of such “gene swapping” took place duringthe early evolution of the prokaryotes. Although TEshave been best studied in prokaryotes, they have beenfound in most organisms that have been examined, in-cluding insects, mammals, flowering plants, sponges,and flatworms. Although we lack specific evidence,there is reason to suspect that TEs could have been re-sponsible for some of the major genetic innovations thathave taken place in the history of life.

Another way in which evolutionary novelties can ariseis through symbiosis. The Russian biologist KonstantinMereschkovsky (1855–1921) developed the “two-plasm”(cell within a cell) theory, claiming that chloroplasts origi-nated from blue-green algae (Cyanobacteria). For thisprocess, he invented the term symbiogenesis. In Chapter5, we describe the symbiogenic origin of the eukaryoticcell, which probably arose by way of incorporation ofonce free-living prokaryotes that came to be what werecognize today as mitochondria, chloroplasts, cilia, fla-gella, and other organelles. Although symbiogenesis isan old idea, it was Lynn Margulis who most vigorouslychampioned it in the twentieth century.

Beyond the origin of the eukaryotic cell, symbiogene-sis may be at work in many other systems, but we havelittle knowledge of how genetic material might beshared by or influenced among animals in such relation-ships. In extremely intimate symbiotic partnerships,however, the two symbionts could have profound effectson each other’s genetic evolution. Many invertebratesare invovled in such relationships, including the coralsand other cnidarians that serve as hosts for symbiotic di-noflagellates (called zooxanthellae) that live within theirtissues. Various animals that harbor (and exploit)tetrodotoxin-secreting bacteria (many chaetognaths, theblue-ringed octopus, a sea star, and a horseshoe crab,and certain tetraodontid fishes), and squids with lumi-nous bacteria, and lichens (an intimate association be-tween fungi and Cyanobacteria or green algae) are otherexamples. That symbionts can affect the evolution oftheir hosts in unexpected ways can be seen in parasitesthat enhance their own chances for survival by alteringaspects of their host’s lives—for example, parasites that

increase the likelihood that their intermediate host willfall prey to their definitive host by changing the interme-diate host’s size, color, biochemistry, or behavior in waysthat make it more vulnerable to predation.

Another revelation in our thinking about macroevo-lution has come from the discovery of homeobox (Hox)genes. These master regulatory genes modulate othersets of developmental genes and, in doing so, “select”the developmental pathways that are followed by di-viding cells. Hox genes have two functions in the earlydevelopment of embryos: (1) they encode short regula-tory proteins that bind to a particular sequences of basesin DNA and either enhance or repress gene expression,and (2) they encode proteins that are expressed in com-plex patterns that determine the basic geometry of theorganism. The term Hox genes refers specifically tothose genes that are clustered in an array on the chro-mosome and function primarily in establishing regionalor segmental identities. In all Metazoa that have beenexamined, regional or segmental specialization is con-trolled by the spatially localized expression of thesegenes, which play crucial roles in determining body pat-terns. They underlie such fundamental attributes as an-terior–posterior differentiation (in both invertebratesand vertebrates) and the positioning of body wall out-growths (e.g., limbs).

Hox genes have been conserved to a remarkable de-gree throughout the animal kingdom, and they are nowknown from all animal phyla that have been examined.There is a striking correlation between the order of thesegenes on their chromosomes and the position of theirexpression in the developing animal along the mainbody axis. Hox proteins regulate the genes that controlthe cellular processes involved in morphogenesis. Indoing so, they demarcate relative positions in animals—they do not specify the precise nature of particular struc-tures. For example, in arthropods, Hox genes regulatewhere body appendages form, and they can either sup-press limb development or modify it (in concert withother regulatory genes) to create unique appendagemorphologies. Mutations in Hox genes, and other de-velopmental genes, can create gross mutations (homeot-ic mutations or homeosis).

There is a growing body of evidence suggesting thatHox genes have played major roles in the evolution ofnew body plans among the Metazoa. The evolutionarypotential of Hox genes lies in their hierarchical and com-binatorial nature. We now know that a single Hox genecan modulate the expression of dozens of interactingdownstream genes, the products of which determinedevelopmental outcomes. Variation in the output ofthese multigene networks can arise at many levels sim-ply through changes in the relative timing of develop-mental gene expression (i.e., by heterochrony; seeChapter 4), or through interactions between genes in theregulatory network. To understand the profound poten-tial of Hox genes to drive evolutionary change, consider


that, within the genome of Drosophila, 85–170 differentgenes are regulated by the product of the Hox geneUltrabithorax (Ubx) alone (Carroll 1995). Changes in theUbx protein could potentially alter the regulation of allthese genes! In some families of sea spiders (Pycno-gonida), Hox gene mutations appear to have producedspurious segment/leg duplications, creating polymer-ous lineages (see Chapter 19). Another example of thepotential of Hox genes is seen in the abdominal limbs ofinsects. Abdominal limbs (“prolegs”) occur on larvae ofvarious insects in several orders, and they are ubiqui-tous in the Lepidoptera (e.g., caterpillars). These limbswere probably present in insect ancestors, hence prolegsmay have reappeared through the de-repression of anancestral limb developmental program (i.e., they are aHox gene mediated atavism). Proleg formation appearsto involve a change in the regulation and expression of asingle gene (abd-A) during embryogenesis.

In summary, the processes of microevolution (e.g.,natural selection) act on individuals and populations,maintain genomic continuity, and create anastomosingpatterns of relationship over time (Figure 1.6). Macro-evolutionary processes (e.g., speciation and extinction),on the other hand, act on species and lineages, disrupt

genomic continuity, and create ascending, bifurcatingpatterns of relationship over time (Figure 1.6). In acladogram of species, the line segments represent theplaces where anagenesis (microevolution) is takingplace within a given species. The nodes in the clado-gram represent macroevolutionary events, speciationand extinction. Although Darwin titled his book On theOrigin of Species, he dealt primarily with the mainte-nance of adaptations. In fact, the nature of the relation-ship between anagenesis and cladogenesis is still notwell understood. Evidence for the disengagement ofnatural selection and speciation comes from the fossilrecord, which suggests that most species do not changesignificantly throughout their existence; rather, they re-main phenotypically stable for millions of years, thenundergo a rapid change in which they essentially “re-place themselves” with one or more new and differentspecies. These new species, in turn, remain phenotypi-cally static for millions more years. The fossil recordsuggests that most species of marine invertebrates per-sist more or less unchanged for 5–10 million years,whereas the time required for significant anatomicalchange seems to be only a few thousand years or less.This idea of speciation in rapid bursts, sandwiched be-

18 CHAPTER ONE

Tim

e

Species 1

A B C D E F G H Individuals

Mating event

Population #1 Population #2

Species 2

DISRUPTION OF

GENETIC CONTINUITY

Stochastic eventthat breaks down genomic homeostasis (can result in extinction or speciation)

Microevolution (Within species evolution)

1. Individuals and populations linked by gene flow (e.g., reproductive ties, dispersion)

2. Process produces pattern of reticulation

3. Acts on individuals (e.g. natural selection)

4. Works to maintain genomic continuity (i.e. evolutionary homeostasis)

5. Creates an anastomosing network

6. Explains anagenesis

Macroevolution (Species/clade evolution)

1. Species linked by speciation events

2. Process produces pattern of bifurcation (“dendrogram”)

3. Acts on species

4. Disrupts genomic continuity

5. Creates hierarchical, diverging network

6. Explains cladogenesis (origin of clades: species and species groups)

Species 1 Species 3 Species 4

Species

2

Species

1

Extinction event (Extinction of species 2)

Anagenesis (Life of species)

Speciation event (Cladogenesis)

Dispersion

Bar

rier

Bar

rier

Bar

rier

Generation

time

Figure 1.6 Microevolution and macroevolution depicted graphically.Thehighlighted portion of the cladogram (on the right) is shown in detail inthe drawing to the left.


tween long periods of species stasis, was explained inthe punctuated equilibrium model of Eldredge andGould (1972).

Biologists are still a long way from understanding allthe causes and mechanisms of the evolutionary process.That evolution has occurred and is occurring is welldocumented and consistent with all of the availabledata. We are developing excellent methods for analyz-ing the patterns or the history of evolution (e.g., phylo-genetics). The current debates concern the process—thenature of the evolutionary mechanisms themselves. Itseems probable that different processes, working at dif-ferent levels, have created the patterns we see in theworld today. Despite the many evolutionary questionscurrently being discussed, and despite whatever evolu-tionary processes are now at work (probably all of theseand other processes are), biologists are quite able to con-tinue their efforts at reconstructing the evolutionary his-tory of life on Earth, because the processes of evolution(whatever they entail) result in new organisms that aredistinct by virtue of various unique new characters orattributes that they have acquired. Their descendants re-tain these attributes and in time acquire still others,which are retained by their descendants. In this fashion,the living world provides us with an analyzable hierar-chical pattern consisting of nested sets of features recog-nizable both in fossils and in living organisms. Thosefeatures, in turn, are the data (i.e., the “characters”) withwhich we can reconstruct a history of the descent of life.We will have much more to say regarding this recon-struction process in the following chapter, because un-derstanding what characters are and how they are eval-uated is fundamental to comparative biology and to anappreciation of the invertebrate world.

A Final Introductory Message to the ReaderIf you have not already done so, please read the Prefaceto this text, which explains this book’s limitations, de-

scribes what it is about, and outlines what sort of infor-mation we intend to convey. Because of our compara-tive approach, it is critical that you become familiar withthe initial chapters (Chapters 1–4) before attempting tostudy and comprehend the sections dealing with indi-vidual animal groups. These first four chapters are de-signed to accomplish several goals: (1) to define somebasic terminology, (2) to introduce a number of impor-tant concepts, and (3) to describe in detail the themesthat we use throughout the rest of the book.

The fundamental theme of this book is evolution,and we approach invertebrate evolution primarilythrough the field of comparative biology . In Chapter 2we provide an explanation of how biologists derive evo-lutionary schemes and classifications, how theoriesabout the phylogeny of animal groups grow andchange, and how the information presented in this texthas been used to construct theories on how life evolvedon Earth. In Chapters 3 and 4 we lay out the fundamen-tal anatomical and morphological designs and develop-mental strategies of invertebrates. Like the features oforganisms, these designs and strategies are not random,but form patterns. Recognition and analysis of thesepatterns constitute the basic building blocks of thisbook. We then proceed in the “animal chapters” to ex-plore the evolution of the invertebrates in light of vari-ous combinations of these basic functional body plansand lifestyles. With this background, you should be ableto follow the evolutionary changes and branchingsamong the invertebrate phyla, their body systems, andtheir various pathways to success on Earth.

Through our approach, we hope to add continuity tothe massive subject of invertebrate zoology, which isoften covered (in texts and lectures) by a sort of “flash-card” method, in which the primary goal is to have thestudent memorize animal names and characteristicsand keep them properly associated, at least until afterthe examination. Thus, we urge you to look back fre-quently at these first few chapters as you read aheadand explore how invertebrates are put together, howthey live, and how they evolved.


Selected ReferencesGeneral ReferencesAdams, E. 1987. Invertebrate collagens. Science 202: 591–598.Barnes, R. D. and E. Ruppert. 1994. Invertebrate Zoology, 6th Ed.

Saunders, Philadelphia.Beklemishev, W. N. 1969. Principles of Comparative Anatomy of

Invertebrates. 2 vols. University of Chicago Press, Chicago.[Translated from Russian; a different view of the subject, quite un-like Western texts.]

Bengtson, S. and Y. Zhao. 1997. Fossilized metazoan embryos from theearliest Cambrian. Science 277: 1645–1648.

Boardman, R. S., A. H. Cheetham and A. J. Rowell. 1987. FossilInvertebrates. Blackwell, London. [A good distillation of fossil in-vertebrate zoology.]

Briggs, D. E. G., D. E. Erwin and F. J. Collier. 1994. The Fossils of theBurgess Shale. Smithsonian Institution Press, Washington, D.C.

Brusca, R. 2000. Unraveling the history of arthropod biodiversifica-tion. Ann. Missouri Bot. Garden 87(1): 13–25.

Buchsbaum, R., M. Buchsbaum, J. Pearse and V. Pearse. 1987. Animalswithout Backbones, 3rd Ed. University of Chicago Press, Chicago.[The third edition of this classic book provides delightful readingand many excellent photographs.]

Carefoot, T. 1977. Pacific Seashores: A Guide to Intertidal Ecology.University of Washington Press, Seattle. [A very clear and readableaccount of ecological concepts as they apply to temperateseashores; the emphasis is on invertebrates.]

Coleman, D. C. and P. F. Hendrix (eds.). 2000. Invertebrates asWebmasters in Ecosystems. Oxford University Press.

Combes, C. 2001. Parasitism: The Ecology and Evolution of IntimateInteractions. University Chicago Press, Chicago. [Brings a unifyingapproach to a subject usually presented in a fragmented fashion.]

Crawford, C. S. 1981. Biology of Desert Invertebrates. Springer-Verlag,New York.

Curtis, T. P., W. T. Sloan and J. W. Scannell. 2002. Estimating prokary-otic diversity and its limits. Proc. Natl. Acad. Sci. U.S.A. 99(16):10494–10499. [Also see comment by B. Ward, same issue,10234–10236.]

Donoghue, M. J. and W. S. Alverson. 2000. A new age of discovery.Ann. Missouri Bot. Garden 87(1): 110–126.

Ekman, S. 1953. Zoogeography of the Sea. Sedgwick and Jackson,London. [Excellent review of marine invertebrate distributions;dated, but a benchmark work.]

Erwin, T. L. 1991. How many species are there? Revisited. Conserv.Biol. 5: 1–4. [See also F. Ødegaard. 2000. How many species ofarthropods? Erwin’s estimate revised. Biol. J. Linn. Soc. 71:583–597.]

Fredrickson, J. K. and T. C. Onstott. 1996. Microbes deep inside theEarth. Sci. Am. 275: 68–73.

Freeman, W. H. and B. Bracegirdle. 1971. An Atlas of InvertebrateStructure. Heinemann Educational Books, London. [A good labo-ratory aid; treats gross morphology, anatomy, and histology, withillustrations and photographs.]

Giese, A. and J. S. Pearse (eds.). 1974–1987. Reproduction of MarineInvertebrates. Vols. 1–5, 9. Academic Press, New York. [With moreon the way; excellent review articles.]

Gilbert, S. F. and A. M. Raunio (eds.). 1997. Embryology: Constructingthe Organism. Sinauer Associates, Sunderland, MA. [The best con-temporary work on the subject.]

Grassé, P. (ed.). 1948. Traité de Zoologie. Masson et Cie, Paris. [Workcontinues on this multivolume enterprise covering the animalkingdom; one of the best single reference sources on invertebrates.]

Hardy, A. C. 1956. The Open Sea. Houghton Mifflin, Boston. [Still thebest introduction to the world of plankton.]

Harrison, F. W. (ed.). 1991–1997. Microscopic Anatomy of Invertebrates.Wiley-Liss, New York. [A 20-book series providing up-to-date, de-tailed treatments of anatomy, histology, and ultrastructure.]

Hawkesworth, D. L. 1995. Biodiversity: Measurement and Estimation.Chapman & Hall, London.

Haywood, V. E. 1996. Global Biodiversity Assessment. CambridgeUniversity Press, Cambridge. [A whole-earth encyclopedia of bio-diversity.]

Hedgpeth, J. W. (ed.). 1957. Treatise on Marine Ecology and Paleoecology.Geological Society of America Memoir 67. [Still frequently consult-ed and cited; excellent reviews of major aspects of marine biology.]

Hoppert, M. and F. Mayer. 1999. Prokaryotes. Amer. Sci. 87: 518–525.Hyman, L. H. 1940–1967. The Invertebrates. 6 vols. McGraw-Hill, New

York. [This series has probably ended. Naturally, some of the ma-terial in early volumes is out of date, but they still remain amongthe best references available.]

Kaestner, A. 1967–1970. Invertebrate Zoology. Vols. 1–3. Wiley-Interscience, New York. [Translated from German.]

King, J. L., M. A. Simovich and R. C. Brusca. 1996. Species richness, en-demism and ecology of crustacean assemblages in northernCalifornia vernal pools. Hydrobiologia 328: 85–116. [A detailedlook at a rare and threatened environment.]

Lankester, R. (ed.). 1900–1909. A Treatise on Zoology. Adam and CharlesBlack, London. [A classic multivolume work on invertebrates.Despite its age, this remains a valuable resource.]

Larwood, G. and B. Rosen (eds.). 1979. Biology and Systematics ofColonial Organisms. Academic Press, New York.

Lincoln, R. J., G. A. Boxshall, and P. F. Clark. 1982. A Dictionary ofEcology, Evolution and Systematics. Cambridge University Press,New York. [Excellent.]

Madigan, M. 2000. Extremophilic bacteria and microbial diversity.Ann. Missouri Bot. Garden 87(1): 3–12.

Madigan, M. and B. Marrs. 1997. Extremophiles. Sci. Am. 276: 82–87.Marshall, N. B. 1980. Deep Sea Biology: Development and Perspective.

Garland STPM Press, New York.Moore, J. 1984. Parasites that change the behavior of their host. Sci.

Am. (May): 108–115.Moore, R. C. (ed.). 1952–present. Treatise on Invertebrate Paleontology.

Geological Society of America and University of Kansas Press,Lawrence. [Detailed coverage of fossil forms; many volumes stillpending.]

Norse, E. (ed.). 1993. Global Marine Biological Diversity. Island Press,Washington, D.C.

Panganiban, G. et al. 1997. The origin and evolution of animal ap-pendages. Proc. Natl. Acad. Sci. U.S.A. 94: 5162–5166.

Parker, S. P. (ed.). 1982. Synopsis and Classification of Living Organisms. 2vols. McGraw-Hill, New York. [Encyclopedic; dry.]

Poore, G. C. B. and G. D. F. Wilson. 1993. Marine species richness.Nature 361: 597–598.

Price, P. W. 1980. Evolutionary Biology of Parasites. Princeton UniversityPress, Princeton, NJ.

Prosser, C. L. (ed.). 1991. Environmental and Metabolic AnimalPhysiology. Wiley-Liss, New York. [One of the best accounts ofcomparative physiology.]

Roberts, L. S. and J. Janovy, Jr. 1996. Foundations of Parasitology, 5th Ed.Wm. C. Brown, Dubuque, IA. [One of the better of a generally dis-appointing field of textbooks on parasitology.]

Sarbu, S. M. and T. C. Kane. 1995. A subterranean chemoautotrophi-cally based ecosystem. NSS Bull. 57: 91–98.

Seilacher, A., P. K. Bose and F. Pflüger. 1998. Triploblastic animals morethan one billion years ago: Trace fossil evidence from India.Science 282: 80–83.

Stachowitsch, M. 1992. The Invertebrates: An Illustrated Glossary. Wiley-Liss, New York.

Stephensen, T. A. and A. Stephensen. 1972. Life Between Tide Marks onRocky Shores. W. H. Freeman, San Francisco. [A summary of the au-thors’ life work on the subject; primarily deals with algae and in-vertebrates; global in coverage.]

Wilson, E. O. 1992. The Diversity of Life. Belknap Press, HarvardUniversity Press, Cambridge, MA. [Outstanding writing by one ofthe greatest living American naturalists.]

Wilson, E. O., and F. M. Peter (eds.). 1988. Biodiversity. NationalAcademy Press, Washington, D.C.

Wray, G. A., J. S. Levinton and L. H. Shapiro. 1996. Molecular evidencefor deep Precambrian divergences among metazoan phyla.Science 274: 568–573.

Zhuravlev, A. and R. Riding (eds.). 2001. The Ecology of the CambrianRadiation. Columbia University Press, New York.

Manuals and Field Guides for Identification of InvertebratesWe have included here only a few of the scores of identification

guides, booklets, and the like. Guides to particular taxa are listedin appropriate chapters.

Allen, G. R. and R. Steene. 1994. Indo-Pacific Coral Reef Field Guide.Tropical Reef Research, Singapore.

Allen, R. 1969. Common Intertidal Invertebrates of Southern California.Peek Publications, Palo Alto, CA. [The only compilation of keys tosouthern California invertebrates ever published; out of print andhard to find.]

Bright, T. J. and L. H. Pequegnat (eds.). 1974. Biota of the West FlowerGarden Bank. Gulf Publishing Co., Houston, TX.

Brusca, G. J. and R. C. Brusca. 1978. A Naturalist’s Seashore Guide:Common Marine Life of the Northern California Coast and AdjacentShores. Mad River Press, Eureka, CA. [Currently being revised.]

Brusca, R. C. 1980. Common Intertidal Invertebrates of the Gulf ofCalifornia, 2nd Ed. University of Arizona Press, Tucson. [A fairlyexhaustive treatment of the subject, including keys, descriptions,and figures for over 1,300 species; currently being revised.]

Colin, P. I. 1978. Caribbean Reef Invertebrates and Plants. T. F. H.Publications, Neptune City, NJ.

Edmondson, W. T., H. B. Ward and G. C. Whipple (eds.). 1959.Freshwater Biology. Wiley, New York. [Good keys to freshwater in-vertebrates.]

Fielding, A. 1982. Hawaiian Reefs and Tidepools. Oriental, Honolulu.Fish, J. D. and S. Fish. 1996. A Student’s Guide to the Seashore, 2nd Ed.

Cambridge University Press, Cambridge. [An excellent survey ofthe invertebrates of British shores.]

Gosliner, T. M., D. W. Behrens and G. C. Williams. 1996. Coral ReefAnimals of the Indo-Pacific. Sea Challengers, Monterey, CA.

Gosner, K. L. 1971. Guide to the Identification of Marine EstuarineInvertebrates. Wiley-Interscience, New York. [For use on the north-eastern coast of the United States.]


Hayward, P. and J. S. Ryland (eds.). 1995. Handbook of the Marine Faunaof North-West Europe. Oxford University Press, Oxford.

Hobson, E. and E. H. Chave. 1990. Hawaiian Reef Animals. Universityof Hawaii Press, Honolulu.

Humann, P. 1992. Reef Creature Identification: Florida, Caribbean,Bahamas. New World Publications, Jacksonville, FL.

Humann, P. 1993. Reef Coral Identification: Florida, Caribbean, Bahamas.New World Publications, Jacksonville, FL.

Kaplan, E. 1982. A Field Guide to Coral Reefs of the Caribbean and Florida.Houghton Mifflin, Boston. [Excellent; one of the Peterson FieldGuides.]

Kozloff, E. 1974. Keys to the Marine Invertebrates of Puget Sound, the SanJuan Archipelago, and Adjacent Regions. University of WashingtonPress, Seattle.

Kozloff, E. 1987. Marine Invertebrates of the Pacific Northwest. Universityof Washington Press, Seattle.

Laboute, P. and Y. Magnier. 1979. Underwater Guide to New Caledonia.Les Editions Pacifique, Papeete, Tahiti.

Luther, W. and K. Fiedler. 1976. A Field Guide to the Mediterranean SeaShore. Collins, London.

McConnaughey, B. H. and E. McConnaughey. 1985. Pacific Coast: TheAudubon Society Nature Guides. Chanticleer Press, New York.

Morris, R. H., D. P. Abbott and E. C. Haderlie. 1980. IntertidalInvertebrates of California. Stanford University Press, Stanford, CA.

Newell, G. and R. Newell. 1973. Marine Plankton: A Practical Guide.Hutchinson, London.

Pennak, R. W. 1989. Fresh-Water Invertebrates of the United States:Protozoa to Mollusca, 3rd Ed. John Wiley & Sons, New York.

Ricketts, E. F., J. Calvin, J. W. Hedgpeth and D. W. Phillips. 1985.Between Pacific Tides, 4th Ed. Stanford University Press, Stanford,CA. [A standard reference for natural history of Pacific coast inter-tidal invertebrates.]

Riedl, R. (ed.). 1983. Fauna und Flora des Mittelmeeres. Verlag PaulParey, Hamburg. [Perhaps the best field guide for theMediterranean.]

Ruppert, E. E. and R. S. Fox. 1988. Seashore Animals of the Southeast: AGuide to Common Shallow-Water Invertebrates of the SoutheasternAtlantic Coast. University of South Carolina Press, Columbia.

Sefton, N. and S. K. Webster. 1986. A Field Guide to Caribbean ReefInvertebrates. Sea Challengers, Monterey, CA.

Smith, R. I., and J. Carlton (eds.). 1975. Light’s Manual: IntertidalInvertebrates of the Central California Coast, 3rd Ed. University ofCalifornia Press, Berkeley. [A product of the editors’ devotion tothe task; includes keys; well referenced.]

Sterrer, W. (ed.). 1986. Marine Fauna and Flora of Bermuda. Wiley, NewYork. [A comprehensive guide.]

Thorp, J. H. and A. P. Covich (eds.). 1991. Ecology and Classification ofNorth American Freshwater Invertebrates. Academic Press, SanDiego, CA.

Todd, C. D., M. S. Laverack and G. A. Boxshall. 1996. Coastal MarineZooplankton, 2nd Ed. Cambridge University Press, Cambridge.

Wirtz, P. 1995. Unterwasserführer Madeira Kanaren/Azoren. VerlagStephanie Naglschmid, Stuttgart. [An underwater guide to theCanary Islands, Azores, and Madeira.]

Some Recommended References on EvolutionAvers, C. J. 1989. Process and Pattern in Evolution. Oxford University

Press, New York.Ayala, F. J. (ed.). 1976. Molecular Evolution. Sinauer Associates,

Sunderland, MA.Ayala, F. J. and J. W. Valentine. 1979. The Theory and Processes of Organic

Evolution. Benjamin/Cummings, Menlo Park, CA.Benton, M. J. 1995. Diversification and extinction in the history of life.

Science 268: 52–58.Berg, D. E. and M. M. Howe (eds.). 1989. Mobile DNA. American

Society of Microbiology, Washington, D.C.Bermudes, D. and L. Margulis. 1987. Symbiont acquisition as

neoseme: Origin of species and higher taxa. Symbiosis 4: 185–198.Brock, J. J., G. A. Logan, R. Buick and R. E. Summons. 1999. Archean

molecular fossils and the early rise of eukaryotes. Science 285:1033–1036.

Brooks, D. R. and E. O. Wiley. 1988. Evolution as Entropy, 2nd Ed.University of Chicago Press, Chicago. [A view of evolution thatchallenges traditional thinking on the subject.]

Bush, G. L. 1975. Modes of animal speciation. Annu. Rev. Ecol. Syst. 6:339–364. [One of the classic review studies on “traditional” specia-tion models.]

Dyer, B. D. and R. Obar (eds.). 1985. The Origin of Eukaryotic Cells: Bench-mark Papers in Systematic and Evolutionary Biology. Van NostrandReinhold, New York.

Eldredge, N. 1982. Phenomenological levels and evolutionary rates.Syst. Zool. 31: 338–347.

Eldredge, N. 1985a. Time Frames. Simon & Schuster, New York. [Withthis book, and a series of subsequent books on macroevolutionarytopics, Eldredge has synthesized many of our changing views onevolution.]

Eldredge, N. 1985b. Unfinished Synthesis: Biological Hierarchies andModern Evolutionary Thought. Oxford University Press, New York.[An important, thought-provoking look at the “modern synthesis”of evolution, its shortcomings, and some alternative ideas on evo-lutionary theory.]

Eldredge, N. 1989. Macroevolutionary Dynamics: Species, Niches, andAdaptive Peaks. McGraw-Hill, New York. [Excellent reading.]

Eldredge, N. 1991. The Miner’s Canary: Unraveling the Mysteries ofExtinction. Princeton University Press, Princeton, NJ.

Eldredge, N. (ed.). 1992. Systematics, Ecology, and the Biodiversity Crisis.Columbia University Press, New York.

Eldredge, N. and S. J. Gould. 1972. Punctuated equilibria: An alterna-tive to phyletic gradualism. In T. J. M. Schopf (ed.), Models inPaleobiology. Freeman, Cooper, San Francisco, pp. 82–115.

Eldredge, N. and S. N. Salthe. 1984. Hierarchy and evolution. In R.Dawkins and M. Ridley (eds.), Oxford Surveys in EvolutionaryBiology, vol. 1. Oxford University Press, Oxford, pp. 182–206.

Eldredge, N. and S. M. Stanley (eds.). 1984. Living Fossils. SpringerVerlag, New York.

Fisher, A. 1989. Endocytobiology: The wheels within wheels in the su-perkingdom Eucaryota. Mosaic 20: 2–13.

Futuyma, D. J. 1986. Evolutionary Biology, 2nd Ed. Sinauer Associates,Sunderland, MA. [An enjoyable approach to the subject; de-em-phasizes phylogeny and macroevolution but excellent on the sub-jects of anagenesis and adaptation.]

Futuyma, D. J. and G. C. Mayer. 1980. Non-allopatric speciation in an-imals. Syst. Zool. 29: 254–271.

Gillespie, J. H. 1991. The Causes of Molecular Evolution. OxfordUniversity Press, New York. [Good background reading for thosewith a serious interest in molecular evolution.]

Gould, S. J. 1977. Ontogeny and Phylogeny. Harvard University Press,Cambridge, MA. [A scholarly treatment of the myriad relation-ships postulated, over the past 100 years, to exist between ontoge-ny and phylogeny, including recapitulation, paedomorphosis, andneoteny; highly recommended. Also see G. J. Nelson’s 1978 article,“Ontogeny, phylogeny, paleontology and the biogenetic law”(Syst. Zool. 27: 324–345).]

Gould, S. J. 1989. Wonderful Life. W.W. Norton, New York.Gould, S. J. and N. Eldridge. 1977. Punctuated equilibria: The tempo

and mode of evolution reconsidered. Paleobiology 3: 115–151.Gould, S. J. and R. C. Lewontin. 1979. The spandrels of San Marco and

the Panglossian paradigm: A critique of the adaptationist pro-gramme. Proc. R. Soc. Lond. Ser. B 205: 581–598. [A highly recom-mended read.]

Gray, J. and W. Shear. 1992. Early life on land. Am. Sci. 80: 444–456.Haeckel, E. 1866. Generelle Morphologie der Organismen. Georg Reimer,

Berlin.Hall, B. K. 1996. Baupläne, phylotypic stages, and constraint: Why are

there so few types of animals? Evol. Biol. 29: 215–257.Hallam, A. 1978. How rare is phyletic gradualism and what is its evo-

lutionary significance? Evidence from Jurassic Bivalvia.Paleobiology 4: 16–25.

Hallam, A. and P. B. Wignall. 1997. Mass Extinctions and TheirAftermath. Oxford University Press, Oxford.

Hsü, K. J. et al. 1982. Mass mortality and its environmental and evolu-tionary consequences. Science 216: 249–256.


Jablonski, D. 1986. Larval ecology and macroevolution in marine in-vertebrates. Bull. Mar. Sci. 39: 565–587.

Kidwell, M. G. 1993. Lateral transfer in natural populations of eukary-otes. Ann. Rev. Genet. 27: 235–256.

Kimura, M. 1983. The Neutral Theory of Molecular Evolution. CambridgeUniversity Press, New York.

Lenski, R. E. and J. E. Mittler. 1993. The directed mutation controversyand neo-Darwinism. Science 259: 188–194.

Levin, D. A. 2000. The Origin, Expansion, and Demise of Plant Species.Oxford Univesity Press, New York.

Lewontin, R. C. 1974. The Genetic Basis of Evolutionary Change.Columbia University Press, New York. [A solid treatment of evolu-tionary genetics.]

Li, W.-H. and D. Graur. 1991. Fundamentals of Molecular Evolution.Sinauer Associates, Sunderland, MA.

Lim, J. K. and M. J. Simmons. 1994. Gross chromosome rearrange-ments mediated by transposable elements in Drosophilamelanogaster. BioEssays 16(4): 269–275.

Lipps, J. H. and P. W. Signor (eds.). 1992. Origin and Early Evolution ofthe Metazoa. Plenum Press, New York. [Excellent contributed chap-ters dealing with the early evolution of Metazoa.]

Lipscomb, D. 1985. The eukaryote kingdoms. Cladistics 1: 127–140.Margulis, L. 1989. Symbiosis in Cell Evolution. W. H. Freeman, San

Francisco.Margulis, L. and R. Fester (eds.). 1991. Symbiosis as a Source of

Evolutionary Innovation: Speciation and Morphogenesis. MIT Press,Cambridge, MA.

Margulis, L. and L. Olendzenski (eds.). 1992. Environmental Evolution:Effects of the Origin and Evolution of Life on Planet Earth. MIT Press,Cambridge, MA.

Margulis, L. and D. Sagan. 1986. Origins of Sex: Three Billion Years ofGenetic Recombination. Yale University Press, New Haven, CT.

Otte, D. and J. A. Endler (eds.). 1989. Speciation and Its Consequences.Sinauer Associates, Sunderland, MA.

Patterson, C. 1999. Evolution. 2nd ed. Cornell University Press, Ithaca,New York. [One of the best, most concise descriptions of evolutionand classification.]

Patterson, C. (ed.). 1987. Molecules and Morphology in Evolution: Conflictor Compromise? Cambridge University Press, Cambridge.

Patterson, C., D. M. Williams and C. J. Humphries. 1993. Congruencebetween molecular and morphological phylogenies. Ann. Rev.Ecol. Syst. 24: 153–188.

Price, P. W. 1980. Evolutionary Biology of Parasites. Princeton UniversityPress, Princeton, NJ.

Radicella, J. P., P. U. Park, and M. S. Fox. 1995. Adaptive mutation inEscherichia coli: A role for conjugation. Science 268:418–420.

[Support for recent, controversial claims that not all mutations arerandom—i.e., the evolutionary watchmaker isn’t always blind!]

Raff, R. A. 1996. The Shape of Life: Genes, Development, and the Evolutionof Animal Form. University of Chicago Press, Chicago.

Raff, R. A. and T. C. Kaufman. 1983. Embryos, Genes, and Evolution.Macmillan, New York. [Excellent reading.]

Raup, D. M. 1983. On the early origins of major biologic groups.Paleobiol. 9: 107–115.

Raup, D.M., S. J. Gould, T. M. Schopf and D. S. Simberloff. 1973.Stochastic models of phylogeny and the evolution of diversity. J.Geol. 81: 525–542.

Raup, D. M. and J. J. Sepkoski. 1982. Mass extinctions in the marinefossil record. Science 215: 1501–1503.

Rensch, B. 1959. Evolution Above the Species Level. Columbia UniversityPress, New York. [The English translation of Rensch’s classic treat-ment of a conceptually challenging subject. Though now showingits age, the original text (1947; 1954) had considerable influence onthe development of modern evolutionary theory.]

Ridley, M. 1996. Evolution. Blackwell Science, Cambridge, MA. [One ofthe best general evolution texts available.]

Schopf, J. W. (ed.). 1983. Earth’s Earliest Biosphere: Its Origin andEvolution. Princeton University Press, Princeton, NJ. [Good reviewof Precambrian biology.]

Schopf, T. M. J. (ed.). 1972. Models in Paleobiology. Freeman, Cooper,San Francisco.

Shixing, Z. and C. Huineng. 1995. Megascopic multicellular organismsfrom the 1700-million-year-old Tuanshanzi Formation in the Jixianarea, north China. Science 270: 620–622.

Stanley, S. M. 1979. Macroevolution: Pattern and Process. W. H. Freeman,San Francisco.

Stanley, S. M. 1982. Macroevolution and the fossil record. Evolution36: 460–473.

Swofford, D. L. 1991. When are phylogeny estimates from molecularand morphological data incongruent? In M. M. Miyamoto and J.Cracraft (eds.), Phylogenetic Analysis of DNA Sequences. OxfordUniversity Press, New York, pp. 295–333.

Woese, C. R. 1981. Archaebacteria. Sci. Am. 244(6): 98–122.Woese, C. R., O. Kandler and M. L. Wheelis. 1990. Towards a natural

system of organisms: Proposal for the domains Archaea, Bacteria,and Eucarya. Proc. Natl. Acad. Sci. U.S.A. 87: 4576–4579.

Wray, G. A., J. S. Levinton and L. H. Shapiro. 1996. Molecular evidencefor deep Precambrian divergences among metazoan phyla.Science 274: 568–573.

[Also see references on evolution at end of Chapter 2.]


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