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Home , Acetes, Actaea (crab), Aega (genus), Alicella, Amphionides, Anaspidacea

rustaceansare one of the most popular invertebrate groups, even amongnonbiologists, for they include someof the world's most delec- table gourmet fare,such as ,, and (Figure 21.1). There are an estimated 70,000described living speciesof Crustacea,and probably five or ten times that number waiting to be discovered and named. They exhibit an incredible diversity of form, habit, and size. The smallest known are less than 100 pm in length and live on the antennules of cope- pods. The largest are Japanesespider crabs (Macrocheiraknempferi),withleg spans of 4m, and giant Tasmanian crabs (Pseudocarcinusgigas) with widths of 46 cm. The heaviest crustaceans are probablv American lobsters (Homarus americanus),which, before the present era of overfishing, attained weights in excessof 20 kilograms. The world's largest land by weight (and possibly the largest land invertebrate) is the (Birgus latro), Classificationof The weighing in at up to 4 kg. Crustaceans are found Kingdom(Metazoa) at all depths in every marine, brackislu and fresh- water envfuonment on Earth, including in pools at Non-* Lophophorata 6,000m elevation (fairy and cladocerans in (a.k.a. the diploblasts) PHYLUM PHORONIDA northem Chile). Afew have become PHYLUM PORIFERA PHYLUM successful on PHYLUM PLACOZOA PHYLUM BRACHIOPODA. land, the mostnotablebeing sowbugs and pillbugs I PHYLUM EcpYsozoA (the terrestrial isopods). PHYLUM Nematoida Crustaceans are commonly the dominant or- PHYLUM NEMATODA Bilateria ganisms in aquatic subterranean ecosystems, and PHYLUM NEMATOMORPHA (a.k.a.the triploblasts) new of these stygobionts continue to be Scalidophora PHYLUM XENACOELOMORPHA discovered as new caves are explored. They also PHYLUM KINORHYNCHA Protostomia PHYLUM PRIAPULA dominate ephemeral pool , where many PHYLUM PHYLUM LORICIFERA undescribed species are known to occur.2 And SprRmn Panarthropoda crustaceans are the mostwidespread, diverse, and PHYLUM PLATYHELMINTHES PHYLUM TARDIGRADA PHYLUM GASTROTRICHA PHYLUM ONYCHOPHORA This chapter has been revised by Richard C. Bruscaand PHYLUM RHOMBOZOA Joel PHYLUM ARTHROPODA W. Martin PHYLUM OBTHONECTIDA SUBPHYLUMcRusrAcEA" lWhen most people hear the word "shrimp" PHYLUM they think of SUBPHYLUM edible shrimps, two crustaceangroups nestedwithin the PHYLUM SUBPHYLUM Decar:oda(in the subordersDendrobranchiata and PHYLUM ANNELIDA SUBPHYLUM CHELICEFATA Pleocyemati).However, the term "shrimp" is applied to a PHYLUM ENTOPROCTA Deuterostomia number of long-tailed crustaceans,many not closely related PHYLUM CYCLIOPHORA PHYLUM ECHINODERMATA at all to decapods.So, in this generalsense, there are fairy tadpole mantis Gnathifera PHYLUM HEMICHORDATA shrimps, shrimps, shrimps, etc. In much of PHYLUM GNATHOSTOMULIDA the English-speakingworld, the word "" is used for PHYLUM CHORDATA PHYLUM MICROGNATHOZOA the edible shrimps, thus eliminating some of the confusion. *Paraphyletic 2One PHYLUM ROTIFERA group study of ephemeralpools in northern dis- covered30 nrobable undescribedand unnamed species(King et al.7996). 762 ChapterTwenty-One

(A) PHYLUMARTHROPODA Crustacea: Crabs, Shrimps, and TheirKin 763 (o)

Figure 21 .1 Diversity among the Crustacea. (A-D) Classes , , and . (A) Spe/eonectes ondinae; note the remarkably homono- vivesi (: ). (M) The Hawaiian regal , mous body of this swimming crustacean (Remipedia). Enoplometopus (Decapoda: ). (N,O) Two unusual (B) A cephalocarid. (C) A tadpole shrimp (Branchiopoda; amphipods (: ). (N) Cysfisoma, a ) from an ephemeral pool. (D) A huge (some exceed 10 cm), transparent, pelagic hyperiid (Branchiopoda: ), carrying . (E-Q) amphipod. (O) Cyamus scammoni, a parasitic caprellid . (E) The fiddler crab, Uca princeps amphipod that lives on the skin of gray whales. (P) A male (Decapoda: Brachyura). (D The giant Caribbean hermit and female cumacean; note the eggs in the marsupium crab, Petrochirus diogenes (Decapoda: ). (G) A of the female (Peracarida: ). (Q) pacifica (Paragiopagurus fasciatus) removed from its (Peracarida: lsopoda), the rock louse; Lrgra are inhabitants shell (Decapoda: Anomura). (H) The , of the high spray zone on rocky shores worldwide. (R) The Birgus latro (Decapoda: Anomura), climbing a . mysid Slriel/a sp. (Peracarida: ) with a parasitic epi- (l) Euceramus praelongus, the New England olive pit caridean isopod (Peracarida: lsopoda: Dajidae) attached to (Decapoda: Anomura). (J) The pelagic lob- its carapace (Western ). (S,T) Class . sterette, planipes (Decapoda: Anomura). (S) Acorn , Semibalanus balanoides (Cirripedia: (K) The cleaner shrimp, californica (Decapoda: ). (l-) anatifera (Cirripedia: Thoracica), a ). (L) The unusual rock-boring lobster shrimp, Axrus pelagic hanging from a floating timber. (Continued on next page) 764 ChapterTwenty-One

Figure 21 .1 (continued) Diversity among the Crustacea. (U) Class Copepoda; the calanoid Gaussra, a common planktonic . (V) Class , Deoterthron, parasitic on other crustaceans. abundant inhabiting the world's oceans.The biomassof one species,the Antarctic (Euphausia superba),has been estimated at 500million tons at any given time, probably surpassingthe biomassof any other group of marine animals (and rivaling that of the BOX21A Characteristicsof the world's ants).The range of morphological diversity among crustaceansfar exceedsthat of even the . SubphylumCrustacea Many speciesof Crustaceaare threatenedby environ- 1. Body composed of a 6-segmented head, or cepha- mental degradation,over 500are listed on the IUCN lon (plus the acron), and a long postcephalic trunk; Red List, and about two dozen are protected by the trunk divided into two more or less distinct tagmata U.S.Environmental ProtectionAgency. Crustaceans (e,9., thorax and abdomen) in all but the remipedes are also the most common invasive invertebrates/and and (Figure21 .2) well over 100species have establishedthemselves in (anterior 2. Cephalon composed of to posterior):pre- marine and estuarinewaters of alone. segmental (indistinguishable)acron, protocerebral Becauseof their taxonomic diversity and numerical segment (lackingappendages), antennularseg- ment, antennal segment, mandibular somite, maxil- abundance,it is often said that crustaceansare the "in- lularysomite, and maxillarysomite; one or more sectsof the sea."We prefer to think of insectsas "crus- anterior thoracomeres may fuse with the head in taceansof the land." And indeed, there is now strong members of some classes (e.9., Remipedia,and phylogenetic evidencethat the insectsarose from a Malacostraca),their forming maxillipeds branch within the Crustacea. 3. Cephalic shield or carapace present (highlyreduced Despitethe enormousmorphological diversity seen in anostracans, amphipods, and isopods) among crustaceans(Figures 21.1" to 21..20),they display 4. Appendages multiarticulate,uniramous or biramous a suite of fundamental unifying features (Box 21A). In 5. Mandibles usually multiarticulatelimbs that function an effort to introduce both the diversity and the unity as biting, piercing, or chewing/grinding jaws of this enormousgroup of ,we first present 6. Gas exchange by aqueous diffusion across special- a classificationand synopsesof the major taxa.We then ized branchial surfaces, either -likestructures or discussthe biology of the group as a whole, drawing specialized regions of the body surface examplesfrom its various members.As you read this 7. Excretion by true nephridial structures (e.9., anten- chapter,we ask that you keep in mind the general ac- nal glands, maxillaryglands) count of the arthropodspresented in Chapter20. B. Both simple ocelli and compound occur in most taxa (not Remipedia),at least at some stage of the life cycle; compound eyes often elevated on stalks Classificationof The Crustacea 9. Gut with digestive ceca Crustaceans have been known to humans since ancient 10. With nauplius (unknown from any other arthro- times and have provided us with sources of both food pod subphylum); development mixed or direcl and legend. It is somewhat comforting to carcinolo- gists (those who study crustaceans) to note that Can- PHYLUM ARTHROPODA Crustacea:Crabs, Shrimps, and TheirKin 765

(A) Tail Abdomen---l fan I l--cephal dllFt|F"L l t- Carapace ,l

Propodus Swimmerets (= pleopods) Dactyl Figure 21 .2 Crustacean external mor- phology: A (Malacostraca, ). (A) External form. Note the fully developed carapace covering the Compound cephalon and thorax. (B) The typical mala- Antennule costracan tail fan (ventral view). Note the. position of the anus on the .

Legs (= pereopods) cer, one of the two invertebrates represented in the zodiac, is a crab (the other, of course, is Scorpio-an- other arthropod). Our modem view of Crustacea as a taxon can be traced to Lamarck's scheme in the early nineteenth century. He recognized most crustaceans as such, but placed the barnacles and a few others in separate groups. For many barnacles were clas- SUBORDERONYCHOCAUDATA CIam shrimps, sified with molluscs because of their thick, calcareous cladocerans(water fleas), and cyclestherians outer shell. Crustacean classification as we know it today was more or less established during the second INFRAORDERSPINICAUDATA CIaM shrimos half of the nineteenth century, although internal revi- (e.9.,Cyzi c us, Eu l i m n ad i a, Im n ad i a, Metal im n ad i a) Martin and Davis (2001)presented an sions continue. INFRAORDERCLADOCEROMORPHA Water fleas readers overview of crustacean classification, and are and cyclestheriids referred to that publication for a window into the laby- rinthine history of this subphylum. Our classification TRIBE CYCLESTHERIDAMonotypic: Cycle- recognizes 1-1-classes, following Ahyong et al. (2011) stheria hislopi and Martin et al. (201.4). TRIBE Water fleas (e.g., Anchistropus, Daphnia, , Moina, Poly- phemus) CLASSIFICATION OF CRUSTACEA CLASSMALACOSTRACA CLASSREMIPEDIA Remipedes. One livingorder, Nec- tiopoda (e.9., Cryptocorynectes,Godzillius, Lasionectes, SUBCLASSPHYLLOCARIDA Pleom oth ra, Spe/eonectes) ORDERLEPTOSTRACA Leotostracans or nebali- CLASSCEPHALoCARIDA Cephalocarids (e.9., Chiltoniella, aceans (e.9., Dahlella,Levinebalia, Nebalia, Neb- Hampsonellus,Hutchinsoniella, Lightiella, Sandersiella) aliel la, Nebaliopsis, Paranebali a) CLASSBRANCHIOPODABranchiooods SUBCLASSHOPLOCARIDA oRDERANoSTRAoA Fairyshrimps (e.9.,Artemia, ORDERSTOMATOPODA Mantis shrimps (e.9., ,Branchinella, ) Echinosquilla,Gonodactylus, Hemisquilla, Squilla) ORDERNOTOSTRACA Tadoole shrimps (Lepidu- SUBCLASSEUMALACOSTMCA rus, ) SUPERORDERSYNCARIDA Syncarids ORDERDIPLOSTRACA The "bivalved"branchio- ORDERBATHYNELLACEA (e.9., Bathynella) oods ORDERANASPIDACEA (e.9., Anaspides,Psam- SUBORDERLAEVICAUDATA F|at-tailed clam maspides) shrimps(e.9., ) 766 ChapterTwenty-One

SUPERORDEREUCARIDA ORDERLOPHOGASTRTDA Lophogastrids (e.9., ph ORDEREUPHAUSIACEA Euphausids, or krill(e.9., Gnatho ausia,Lophogaster) Bentheuphausia,Euphausia, Meganyctiphanes, ORDERCUMACEA Cumaceans (e.9., Campylaspis, Nyctiphanes) Cumopsis,Diastylis, Diastylopsis) ORDERAMPHIONIDACEAAmphionids. Monotypic: ORDERTANAIDACEA Tanaids (e.9., Apseudes, Amphionidpsreynaudii Heterotanais,Paratanais, ) ORDERDECAPODA Crabs, shrimps, lobsters, etc. ORDERMfCTACEA Mictaceans (e.9., , SUBORDERDENDROBRANCHIATA Penaeid etc.).Some researchers separate out the Hirsutiidae (Bochusacea, and sergestidshrimps (e.9., , , as a distinctorder contain- Sergesfes,) ing Hirsutia,Montucaris and Thetispelecaris). SUBORDERPLEOCYEMATA ORDERSPELAEOGRIPHACEA Spelaeogripha- ceans.Four describedliving species (Potiicoara INFRAORDERCARIDEA Caridean and procarid- brazilienses,Spelaeogriphus lepidops, and two spe- ean shrimps(e.9., Alpheus, Crangon, Hippolyte, ciesof Mangkurtu),and two knownfossil species Lysmata,Macrobrachium, Palaemon, Pandalus, (theCarboniferous Acadiocaris novascofba and the Pasiphaea) UpperJurassic Liaoningogriphus quadripartitus) INFRAORDERPROCARlDOlDA "Primitive" shrimp ORDERTHERMOSBAENACEA Thermosbaena- (Procari s, Vetericaris) ceans(e.9., Halosbaena, Limnosbaena, Monodella, Theosbaena,Thermosbaena, Tulumella) INFRAORDERSTENOPODTDEA Stenopodidean shrimps(e.9., Sponglcola, Stenopus) ORDERISOPODA lsopods (sea slaters, rock lice, pillbugs,sowbugs, roly-polies) INFRAORDERGLYPHEIDEA,.Primitive,, Iobsters (Neoglyphea,Lau rentaegly phea) SUBoRDERANTHURTDEA (e.g., Anthura, Colanthu ra, Cyathu ra, Mesanth ra) INFRAORDERPOLYCHELIDA Deep-sea slipper u lobsters(e.9., Polycheles, Stereomasfis) SUBORDERASELLOTA (e.9., Ase//us, Eurycope, ,Janira, Microcerberus, INFRAORDERBRACHYURA "True" crabs (e.9., Munna) Actaea,Callinectes, Cancer, Cardisoma, Carcinus, SUBORDERCALABOZOIDEA (Calabozoa) Grapsus,Hemigrapsus, Maja, , Ocypode, Pachygrapsus,, Polydectus, Portunus, SUBORDERCYMOTHOIDA (e.g., Aega, Scylla,Uca, Xantho) Bathynomus,, Cirolana, Rocinela) (e.9., INFRAORDERANOMURA Hermit crabs, galatheid SUBORDEREPICARIDEA Bopyrus,Dajus, Hem crabs,sand crabs,porcelain crabs, etc. (e.9., iarthru s, lone, Pseudio ne) Birgus,, Emerita, Galathea, Hippa, Kiwa, SUBORDERGNATHIIDEA (e.9., , Para- Lithodes,Lomis, Paguristes,Pagurus, Petrochirus, gnathia) ,Pleuroncodes, Pylopagurus) SUBORDERLfMNORIDEA (e.9., , Keu- INFMORDERASTACTDEACrayfishes and clawed phylia,Hadromastax) (chelate)lobsters (e.9., Astacus, Cambarus, Homarus,Nephrops) SUBORDER MICROCERBERIDEA(e.9, Atlantase II u s, Mi c roc e rbe r u s) INFRAORDERACHELATA (formerly Palinura). Palinurid,spiny, and Spanish(slipper) lobsters SUBORDERoNISCIDEA (e.9., , (e.9., Enoplometopus,Evibacus, lbacus, , Ligia, Oniscus,, Trichoniscus, , ,Palinurus, Panulirus, Scyllarus) ) INFRAORDERAXIIDEA Lobster shrimos SUBORDERPHREATOICIDEA (e.9., Mesam- phisopus, (e.9.,Axiopsis, Axius, Calocarides,Calocaris, Phreatoicopis,Phreatoicus) Callianassa,iVeaxrus) SUBORDERPHORATOPIDEA (Phoratopus) INFRAORDERGEBIIDEA Mud and ghost shrimps SUBoRDERSPHAEROMATTDEA (e.9., Ancinus, (e.9.,Axianassa, Gebiacantha, Thalassi na, Upo- Bathycopea,Paracerceis, Paradella, Sphaeroma, gebia) Sero/b,Tecticeps) SUPERORDERPERACARIDA SUBORDER TAINISOPIDEA(Pygolabis, oRDERMYSTDA Mysids or opossumshrimps (e.9., Tainisopus\ Acanthomysis,Hemimysis, Mysis, ) SUBORDERVALVIFERA (e.9., Arcturus, ldotea, ) PHYLUMARTHROPODA Crustacea: Crabs, Shrimps, and TheirKin 767

ORDERAMPHIPODA Amphipods-beach hoppers, SUBCLASSNEOCOPEPODA shrimps,whale lice, etc. sandfleas, scuds, skeleton SUPERORDERGYMNOPLEA (e.9., Ampithoe, SUBORDER ORDERCALANOIDA Calanoids (e.9., Bathycalanus, Anisogammarus, Corophium, Eurythenes, ,, Eucalanus,Euchaeta) ,Niphargus, Orchestia, Phoxocephalus, Talitrus) SUPERORDERPODOPLEA SUBORDERHYPERIIDEA (e.9., Cystisoma, oRDERcYcLoPolDA Cyclopoids(e.9., Cyclopina, ,, Primno, Rhabdosoma, Scrna, , Eucyclops, Lernaea, , Streetsia,Vibilia) Notodelphys) SUBORDERCAPRELLIDEA (e.9., , ORDERGELYELLOIDA Gelyelloids (e.9., Gelyella) Cyamus,Metacaprella, Phtisica, Syncyamus) ORDERHARPACTICOIDA Harpacticoids (e.9., Harp- SUBORDERINGOLFIELLIDEA (e.9., lngolfiella, acticus, , Peltidium, Porcellidium, Metaingolfiella) P samm us, Sunarisfes,Ilbbe) CLASSTHECOSTRACA Barnacles and their kin ORDERMISOPHRIoIDA Misophriods (e.9., Box- shallia, Misophria) SUBCLASSFACETOTECTA Monogeneric (Hansenoca- ris):the mysterious"y-larvae," a groupof marinenauplii ORDERMONSTRILLOIDA Monstrilloids (e.9., Mon- andcyprids for which adults are unknown strilla,Stilloma) SUBCLASSASCOTHORACIDA Two orders(, ORDER MORMONILLOIDA Mormonilloids. Dendrogastrida)of parasiticthecostracans (e.9., Asco- Monogeneric: Mormonilla tho rax, Dend ro g aster,Lau ra, Syn ag o g a, Zoanthoec u s) ORDERPOECILOSTOMATOIDA Poecilostoma- SUBCLASSCIRRIPEDIA Cirripedes, the barnacles,and toids (e.9.,, Erebonaster, Ergasilus, theirkin Pseudanthessrus) SUPERORDERTHORACICATruebarnacles. Four or- ORDER SIPHONOSTOMATOIDASiPhONOSIO- ders, (pedunculate or goosebarnacles: matoids (e.g., Clavella, Nernesis, Penella, e.9., Lepas),lbliformes, Scalpelliformes (Pol/atpes, PontoecielIa, Trebiu s) Scalpellum),and (sessile or acornbarnacles: CLASSOSTRACODAOstracods e.9.,Balanus, Chthamalus, , Coronula, Tetraclita,Verruca) SUBCLASSMYODOCOPA SUPERORDERACROTHORACICA Burrowing "bar- ORDER MYODOCOPIDA (e.g., Cypridina, nacles."Two orders, Cryptophialida and Lythoglyptida Euphilomedes, Eusarsiella, Gigantocypris, (e.9.,C ry pto p h i al u s, Trypetesa) Skogsbergia, Vargula) SUPERORDER PATASitiC,,bATNA- ORDER HALOCYPRIDA (e,9., Conchoecia, cles."Two orders,Kentrogonida and Akentrogonida Polycope) (e. Heterosacc u s, Lern aeod isc u s, Mycetom o rp h a, 9., SUBCLASSPODOCOPA Peltogaster,Saccu Ii na, Sylon) ORDERPODOCOPIDA (e.g., Cypris, , CLASSTANTULOCARIDA Deep water, marine parasites Celtia, Darwinula, Lim nocyth re) (e.9.,Bas ipod e I I a, Deoterth ro n, Mi c rod aj u s) ORDERPLATCOP|DA (e.9., Cytherella,Sclero- CLASSBRANCHIURA lice, or argulids.A singlefam- cypris) ily (Argulidae)(e.S., Argulus, Chonopeltis, Dipteropeltis, Dolops) ORDERPALAEOCOPIDA (e.9., Manawa) CLASSPENTASTOMIDA Tongueworms. Two orders,nu- merousfamilies (e.9., Cephalobaena, Linguatula, Pentas- toma, Waddycephalus) Synopses of Crustacean Taxa cLAsS MYSTAoooARIDAMystacocarids, with a single The following descriptions of major crustacean taxa family(Derocheilocarididae), and 13 species(e.9., Cteno- will give you an idea of the range of diversity within chei I o cari s, Dero c h e i I ocari s) the group and the variety of ways in which these suc- cessful animals have exploited the basic crustacean CLASSCOPEPODA . SUBCLASSPROGYMNOPLEA SubphylumCrustacea ORDERPLATYCOPIOIDA Platycopioids (e.9., Antri- Bodycomposed of a 6-segmentedcephalon (plus pre- socopia,Platycopia) segmental acron), or head, and multisegmented post- 768 Chaoter Twentv-One

cephalic trunk; trunk divided into thorax and abdo- The discovery of living remipedes in 1981 by ]ill men (except in remipedes and ostracods); segments of Yager, strange vermiform crustaceans first collected cephalon bear first antennae (antennules), second an- from a cavern in , gave the carcinological tennae, mandibles, maxillules, and maxillae (see Table world a hrm. The combination of features distinguish- 20.2); one or more anterior thoracomeres may fuse with ing these creatures ispuzzling, for they possess charac- the head (e.g., Remipedia and Malacostraca), their ap- teristics that are certainly very primitive (e.g., long, ho- pendages forming'maxillipeds (secondarily modified monomous trunk; double ventral nerve cord; segmental for feeding); cephalic shield or carapace present (sec- digestive ceca;cephalic shield) as well as some athibutes ondarily lost in some groups); with antennal glands traditionally recognized as advanced (e.g., maxillipeds; or maxillary glands (excretory nephridia); both simple nonphyllopodous [though flattened], biramous limbs). ocelli and compound eyes in most groups, at least at They swim about on their backs as a result of metachro- some stage of the life cycle; compound eyes stalked in nalbeating of the trunk appendages, similar to anostra- many groups; with nauplius larval stage (suppressed cans. The remipedes are thus reminiscent of two other or bypassed in some groups), and often a series of ad- primitive classes,the branchiopods and cephalocarids. ditional larval stages. There are an estimated 70,000 F{owever, the laterally directed limbs are unlike those of living species,in over 1,000families.3 any other crustacean/ and the "intemalized" mandibles and the -injecting hypodermic maxillules are Class Remipedia unique (the complex venom contains neurotoxins, pep- Body of two regions, a cephalon and an elongate ho- tidases, and chitinases). The presence of the preanten- monomous trunk of up to 32 segments, each with a nular processes is also puzzling, although similar struc- pair of flattened limbs. Cephalon with a pair of sen- tures are known to occur in a few other crustaceans. sory preantennular frontal processes; first antennae Some phylogenetic analyses based on morphological biramous; trunk limbs laterally directed, biramous, data suggest that remipedes may be the most primitive paddle-like, but without large epipods; rami of trunk living crustaceans, whereas molecular data remain am- limbs (exopod and endopod) each of three or more biguous on the subject or, in some cases,ally them with articles; without a carapace, but with cephalic shield cephalocarids andlor the Hexapoda. covering head; midgut with serially arranged digestive All of the living remipedes discovered thus far are ceca; first trunk segment fused with head and bearing found in caves (usually with connections to the sea) one pair of prehensile maxillipeds; labrum very large, in the Caribbean Basin, , , forming a chamber (atrium oris) in which reside the and Australia. The water in these caves is often dis- "internalized" mandibles; maxillules function as hypo- tinctly stratified, with a layer of fresh water overlying dermic fangs; last trunk segment partly fused dorsally the denser salt water in which the remipedes swim. with telson; telsonwith caudal rami; segmental double Remipedes hatch as lecithotrophic naupliar larvae, ventral nerve cord; eyes absent in living species; male which is also unusual given their (most cave gonopore on trunk limb 15, female on 8; up to 45 mm crustaceans have direct development). Postnaupliar in length. The above diagnosis is for the 24 known liv- development is largely anamorphic; juveniles have ing remipedes (order Nectiopoda); the record is fewer trunk segments than do the adults. Based on the currentlybased on a single poorly preserved specimen three pairs of raptorial, prehensile cephalic limbs (and (order Enantiopoda) (Figures 27.7A 27.3D-F, 27.21D, direct observations), it was long thought that remi- 21..22F,and 21.31E,F). pedes were strictly predators. However, studies by Stefan Koenemann and his colleagues have suggested they might also be capable of suspension feeding. 3Segments of the thorax are called thoracomeres (regardless of whether or not any of these segments are fused to the head), Class Cephalocarida whereas appendages of the thorax are called thoracopods. The term "oereon" refers to that oortion of the thorax not fused to Head followed by 8-segmented thorax with each seg- the heid (when such fusion occurs), and the terms "pereonites" ment bearing limbs, a 11-segmented limbless abdomen, (= pereomeres) and "pereopods" are used for the segments and appendages, respectiveiy, of the pereon. Hence, on a crustacean and a telson with caudal rami; common gonopore on with the first thoracic segment (thoracomere 1) fused to the head, protopods of sixth thoracopods; carapace absent but thoracomere 2 is typically called pereonite 1, the first pair of head covered by cephalic shield; thoracopods 1*7bira- pereopods represents the second pair of thoracopods, and so on. Be assured that we are trying to simplify, not confuse, this issue. mous and phyllopodous, with large flattened exopods Also, we caution you that the of the thorax and abdo- and epipods (exites) and stenopodous endopods; tho- men among the major crustacean lineages is probably more reverie racopods 8 reduced or absent; maxillae resemble thora- than reality; the segmental homologies of the thorax and abdomen have not yet been unraveled among the crustacean classes. For copods; no maxillipeds; eyes absen! nauplii with anten- summaries of naupliar development across the group and iarval nal glands, adults with maxillary glands and (vestigial) features in all crustaceans, see Martin et al. (2014). In most crusta- antennal glands (Figures 21.1T,21.3A-C, and 27.21A). cean species the number of body segments is fixed, but in at least two groups (notostracans and remipedes) the segment number can Cephalocarids are tiny, elongate crustaceansrang- vary within a given species. ing in length from2 to 4 mm. There are 12 species in .=-Protopod Figure 21 .3 Anatomy in the classes Remipedia and Cephalocarida. (A) The cephalocarid H utch i nsoniel la (lat- eral view). (B) SEM of head and thorax of a cephalocarid. (C) First trunk limb of the cephalocarid, Lightiella. (D) The remipede, Spe/eonecfes (ventral view). (E) Tenth trunk limb of the remipede, Lasionecfes. (F) The anterior end of a remipede (ventral view). In both the cephalocarids and the remipedes, the trunk is a long, homonomous series of somites with biramous swimming appendages. In cepha- locarids the first trunk appendages are like all the others, which bear large swimming epipods (exites). In remipedes the first trunk somite is fused to the head, and its append- ages are maxillipeds.

zone to depths of over 1,500m, from the North and South Pacific,to the North and South Atlantic, and the Mediterranean.Hatching is at a slightly advanced naupliar stage(called a metanauplius).Most research- ers agreethat cephalocaridsare very primitive crusta- ceans,largely becauseof their relatively homonomous body form, undifferentiated maxillae, long and gradu- al (anamorphic)larval development, and shapeof the trunk limbs (from which limbs of all other crustaceans seemto be easilyderived).

Class Branchiopoda Number of segmentsand appendageson thorax and abdomen vary, the latter usually lacking appendages; 5 genera. All are benthic marine feeders. Most carapacepresent or absent;telson usually with caudal are associated with sediments covered by a layer of rami; body appendagesgenerally phyllopodous; max- flocculent organic detritus, although some have been illules and maxillae reduced or absent;no maxillipeds found in clean sands. They occur from the intertidal (Figures21..IC,D, 21.4, 21.218, 2L37C, and 21.35B). 770 Chapter Twenty-One

(A)

(F)

Digestive cecum

Food shing

Heart

Rostrum Carapace Antennule Brood chamber Labrum Shell gland Midgut Thoracic Abdominal Postabdominal Processes

Postabdomen

Compound eye 0)

Sensoryfield

Antenna

Rostrum

First thoracopod (modified as a clasper)

Carapace Opercular lamellae (she11) (covering anal somite) Cercopods (=caudal rami) PHYLUM ARTHROPODA Crustacea:Crabs, Shrimps, and TheirKin 771

Compound eyes

Subfrontal plate

Food groove Row of eftes

Egg pouch of eleventh hunk appendage

Abdominal phyllopodia

Caudal ramus

Mandible

Anal somiie

Figure 21 .4 Anatomy and diversity in the class Branchiopoda. (A) An anostracan (Branchinecta) in swim- ming posture. (B) The anostracan, Branchipus schaefferi swimming. (C) Trunk limb of an anostracan (Linderiella). (D,E) The notostracan, Triops: (D) dorsal and (E) ventral views. (F,G) Two cladocerans: (F) Daphnia and (G) Lep- todora. (H) The shed carapace, or ephippium, ot Daphnia, with the embryos enclosed. (l) Two extreme stages in the seasonal change in head form of Daphnia (cyclomorpho- sis). (J-L) The clam shrimp (Diplostraca), Lynceus: (J) the valves are partially open (ventral view); (K) the head (ventral view); (L) the whole animal, with one valve removed. (M) The clam shrimp (Cyclestherida), Cyclestheria, SEM Carapace photo, with one valve removed (the specimen is slightly (shell) distorted; in life the shell is round). 772 Chapter Twentv-One years or decadesuntil the next adequaterains appear. Triopsidae.Most speciesare 2-10 cm long. The com- As diverse as the branchiopods might appear,both mon name derivesfrom the generalbody shape:the morphological and molecular analysesindicate that broad carapaceand narrow "trrtrk" give the animals a they comprise a monophyletic group. Development superficialtadpole-Iike appearance. is remarkably uniform acrossthe group, with naupli- Notostracansinhabit inland waters of all salinities, ar larvae distinguishableby severalunique features. but none occur in the ocean.Of the two known gen- Severaltaxonomft nameshave beenproposed to clus- eta, Triops(Figure 21.4D,E)lives only in temporary ter alleged sister-groupswithin the Branchiopoda,but waters, and its eggsare capableof surviving extended there is as yet little consensus,and branchiopod rela- dry periods.Most speciesof Lepiduruslive in tempo- tionships remain unsettled.Nearly 1,000extant species rary ponds,but at leastone species(L. arcticus)inhab- have been described,and at leastone fossilbranchio- its permanentponds and lakes.However, all species pod(Rehbachiella)is knownfrom the middle , are short-lived, and most completetheir lifecycle in confirming that they are an ancientgroup. just 30 to 40 days. Triopsis of someeconomic impor- tancein that large populations often occur in rice pad- Order Postcephalictrunk divisible into dies and destroy the crop by burrowing into the mud appendage-bearingthorax of 11segments (17 or 19in and dislodging young plants. Tadpole shrimps mosily members of the family Polyartemiidae)and abdomen crawl, but they are also capableof swimming for short of 8 segmentsplus telsonwith caudal rami; gono- periods by beating the thoracic limbs. They are om- pores on genital region of abdomen;trunk limbs bira- nivorous, feeding mostly on organic material stirred mous and phyllopodous; small cephalicshield pres- up from the sediments,although some scavengeor ent; paired, large, stalked compound eyesand a single prey on other animals,including molluscs,other crus- median simple (naupliar) eye. taceans,frog eggs,and even frog tadpolesand small The anostracansare commonly called fairy shrimps .Some species of notostracansare exclusively and brine shrimps. They differ from other branchio- gonochoristic,but others may include hermaphroditic pods in lacking a carapace.There arejust over 300liv- populations (often thosepopulations living at high lat- ing speciesin the order, worldwide, most of which are itudes). Earlier reports of parthenogeneticpopulations less than 1 cm in length, although a few giants attain have been questioned. lengths of 10 cm. Theseanimals inhabit ephemeral ponds (including snowmelt ponds and desertpools), Order Diplostraca The clam shrimps and cladocer- hypersaline lakes, and marine .In many areas ans(water fleas)comprise two groups of closelyrelated they are an important food resourcefor water . branchiopodsknown as the Diplostraca (Figure21.4J- Anostracansare sometimesunited with the extinct L). They sharethe feature of a uniquely developed, order Lipostracaas the subclassSarsostraca. Their fos- large,"bivalved" carapacethat coversall or most of the sil record datesback to the . body. Most diplostracansare benthic, but many swim Anostracansswim ventral side up bv metachronal during reproductive periods. Someare direct suspen- beating of the trunk appendages.Many use theselimb sion feeders,whereas others stir up detritus from the movementsfor suspensionfeeding. Some other spe- substratum and feed on suspendedparticles, and oth- ciesscrape organic material from submergedsurfaces, ers scrapepieces of food from the sediment. and at leasttwo species(Branchinecta gigas, B. raptor) The speciesformerly lumped together as clam are specializedas predators on other fairy shrimps. shrimps are now partitioned between the two diplos- Although most anostracanslive in isolatedponds, their tracan suborders, Laevicaudata and Onychocaudata. eggsmight be transported during passagethrough the Diplostracansshare several features: body divided into gut of predatory divingbeetles (Dytiscidae). cephalonand trunk, the latter with 10-32segments, all with appendages,and with no regionalizationinto tho- Order Notostraca Thoraxof 11segments, each with rax and abdomen;trunk limbs phyllopodous, decreas- a pair of phyllopodous appendages;abdomen of ing in sizeposteriorly; males with trunk limbs 1, or 7-2, "rings," each formed of more than one true segment; modified for grasping females during mating; trunk eachanterior ring with severalpairs of appendages; typically terminates in spinous anal somite or telson, posterior rings lack appendages;telson with long cau- usually with robust caudal rami (cercopods);gono- dal rami; gonoporeson last thoracomere;broad, shield- pores on eleventhtrunk segment;bivalved carapace like carapacefused only with head,but extendingto completelyencloses body; valvesfolded (Spinicaudata, loosely cover thorax and part of abdomenipaired, ses- Cyclestherida)or hinged (Laevicaudata)dorsally; usu- sile compound eyesand a single simple eye near ante- ally with a pair of sessilecompound eyesand a single, rior midline on carapace. median,simple eye. Notostracansare often called tadpole shrimps. The Laevicatdata, or flat-tailed clam shrimps, con- There are only about a dozen living species,in two tains the single family , with close to 40 genera(Triops andLepidurus) placed in a single farnlly, speciesin three genera,characterized by a hinged, PHYLUMARTHROPODA Crustacea: Crabs, Shrimps, and TheirKin 773 globular carapace that encloses the entire animal. The is ectoparasitic on Hydra. Most of the benthic forms Onychocaudata contains the spiny-tailed or "true" feed by scraping organic material from sediment par- clam shrimp in the infraorder Spinicaudata, and the ticles or other objects; the planktonic species are sus- cladocerans (commonly called water fleas) in the pension feeders. Some (e.g., Leptodora,Bythotrephes) are infraorder Cladoceromorpha. Spinicaudatans in- predators on other cladocerans. clude the commonly encountered freshwater genera In , fertllization generally oc- Limnadia, Eulimnidia, Leptestheria, and . The curs in a brood chamber between the dorsal surface of Cladoceromorpha contains the well-known cladoc- the trunk and the inside of the carapace. Most species eran water fleas Daphnia, Moina, Diaphonosoma,and have direct development. In the family Daphnidae the Leptodora, as well as the unique genus Cyclestheria (in developing embryos are retained by a portion of the the Cyclestherida). Confusingly, Cyclestheriais also shed carapace, which functions as an case called an commonly called a clam shrimp, though it is more ephippium (Figure 21..4H),whereas in the closely related to the water fleas). the ephippium remains attached to the entire shed The common name "clam shrimo" derives from the carapace. Leptodora exhibits a heterogenous life cycle, clamlike appearance of the valves, which usually bear altemating between parthenogenesis and sexual repro- concentric growth lines reminiscent of bivalved mol- duction, the latter of which results in free-living larvae luscs. The approximately 200 species of clam shrimps (metanauplii hatch from the shed resting eggs). (including laevicaudatans, spinicaudatans, and Cladoceran life histories are often compared with Cyclestheria)live primarily in ephemeral freshwater those of animals such as rotifers and aphids. Dwarf habitats worldwide. Cyclestheriahislopi,the only mem- males occur in many species in all three groups, and ber of the Cyclestherida, inhabits permanent freshwa- parthenogenesis is common. Members of two cladoc- ter habitats throughout the world's tropics, and is one eran families that undergo parthenogenesis ( of the most widespread animals on Earth. Cyclestheria and Polyphemidae) produce eggs with very little yolk. is also the only clam shrimp with direct development, In these groups the floor of the brood chamber is lined the larval and juvenile stages being passed within the with glandular tissue that secretes a fluid rich in nu- brood chamber, one of the features allying it with the trients, which is absorbed by the developing embryos. cladocerans. Periods of overcrowding, adverse temperatures/ or In cladocerans, the carapace is never hinged (only food scarcity can induce parthenogenetic females to folded dorsally, like a taco) and never covers the entire produce male offspring. Occasional periods of sexual body, and appendages do not occur on all the trunk reproduction have been shown to occur in most par- somites. The body segmentation is generally reduced. thenogenetic species. Many planktonic cladocerans The thorax and abdomen are fused as a "trunk" bear- undergo seasonal changes in body form through suc- ing 4-6 pairs of appendages anteriorly and terminat- ceeding generations of parthenogenetically produced ing in a flexed "postabdomen" with clawlike caudal individuals, a phenomenon known as cyclomorphism rami. Trunk appendages are usually phyllopodous. (Figure 21,.4I). The carapace usually encloses the entire trunk, but not the cephalon, serving as a brood chamber (and greatly Class Malacostraca reduced to this function) in some species; a single me- Body of 19-20 segments, including 6-segmented ceph- dian compound eye is always present. alon, 8-segmented thorax, and 6-segmented pleon The cladocerans, or water fleas, include about 400 (7-segmented in leptostracans), plus telson; with or species of predominantly freshwater crustaceans, al- without caudal rami; carapace covering part or all though several American marine genera and species of thorax, or reduced, or absent; 0-3 pairs of maxil- are known (e.9., Eaadne,Podon). Although there are lipeds; thoracopods primitively biramous, uniramous relatively few species, the group exhibits great mor- in some groups/ phyllopodous only in members of the phological and ecological diversity. Most cladocerans subclass ; antennules and antennae usu- are 0.5-3 mm long, butLeptodorakindtii reaches18 mm ally biramous; abdomen (pleon) usually with 5 pairs in length. Except for the cephalon and large natatory of biramous pleopods and 1 pair of biramous uropods; antennae, the body is enclosed by a folded carapace, eyes usually present, compound, stalked or sessile; which is fused with at least some of the trunk region. mainly gonochoristic; female gonopores on sixth, and The carapace is greatly reduced in members of the male pores on eighth thoracomeres. \Alhen uropods are families Polyphemidae and Leptodoridae, in which it present, they are often broad and flat, lying alongside forms a brood chamber. the broad telson to form a tail fan. Cladocerans are distributed worldwide in nearly all Most classification schemes divide the more than inland waters. Most are benthic crawlers or burrowers; 40,200species of malacostracans into three subclasses, others are planktonic and swim by means of their large Phyllocarida (leptostracans), (stomato- antennae. One genus (Scapholeberis)is typically found pods), and the megadiverse . The in the surface film of ponds, and another (Anchistropus) phyllocarids are typically viewed as representing the 774 ChapterTwenty-One

(A)

Adductor Ovary Maxillary palp venmal nerve cord Hindgut Compound eye

Seventh abdominal Roshum segment pleopod -Fifth Antennal gland Endopod

Antennule First pleopod

Thoracopods

Figure 21 .5 Anatomy in leptostracans (class Malacostraca, subclass Phyllocarida). (A) General anatomy of Nebalia. (B) Phyllopodous swimming limb of Nebalia. (C) SEM ot Nebalia. (D) Anterior end of an oviger- ous Nebalia.

primitive malacostracancondition (6-8-7body seg- ments plus telson;Figure 21.5).The basiceumalacos- tracan body plan, characterizedby the 6-8-6(plus tel- son) arrangementof body segments,was recognized in the early 1900sby W.T. Calman,who termed the defining features of the Eumalacostraca"caridoid fa- cies" (Figure 27.6).Much work has been done since Calman's day, but the basicelements of his caridoid thorax and compressed laterally so as to from an faciesare still presentin all membersof the subclass unhinged bivalved "sheIl," with an adductor muscle; Eumalacostraca. cephalon with a movable, articulated rostrum; pleo- pods 1-4 similar and biramous, 5-6 uniramous; no uro- Subclass Phyllocarida pods; paired stalked compound eyes; antennules bira- Order With the typical malacostracan mous; antennae uniramous; adults with both antennal characteristics,except notable for presenceof seven and maxillary glands (Figures 21.5 and 27.21C). free plpomeres (plus telson) rather than six, generally The subclass Phyllocarida includes about 40 species taken to representthe primitive condition for the class. in 10 genera. Most are 5-15 mm long, butNebiliopsis Also, with phyllopodous thoracopods(all similar to typicais a giant at nearly 5 cm in length. The leptostra- one another); no maxillipeds; large carapacecovering can body form is distinctive, with its loose bivalved

Cephalothorax

Thoracic Figure 21 .6 The basic eumalacostran Carapace somites body plan and the "caridoid facies." Note the thick (muscled)abdomen and j\i.-, Antennule the tail fan, which work in combination :ii :z'tti to produce a powedul tail flip escape r!: reaction. Antennal scale Telson r-x Mandible Tail 'fan ( LY Pleopods PHYLUM ARTHROPODA CrustACEA:CrAbS, Shrimps,and TheirKin 775

(B) Compound eye Carapace Antennule

Antenna Antennal scale

Penis o#".fhs Pleopods Eighth/ / thoracopod Legs3-5 (secondthoracoPod) (gnathopods)

Thoracomeres Cephalon Antennule

Pleotelson

Rudimentary pleopods

2-8 Cephalon [-Thoracomeres

Antenna Maxilliped

Figure 21 -7 External anatomy in the class Malacostraca, subclass Eumalacostraca-stomatopods and syncarids. (A) The spiny Hawaiian stomatopod Echinosquilla guerinii. (B) External anatomy of the stomatopod Squilla. (C) "Spearing" claw and "clubbing" claw (second thoracopod) of stomatopods. (D) A bathynellacean, Bathynella. (E) An anaspidacean, Stygocarella. carapacecovering the thorax, a protruding rostrum, Subclass Hoplocarida and an elongateabdomen. All leptostracansare ma- Order Stomatopoda Carapacecovering portion of rine, and most are epibenthic from the intertidal zone headand fused with thoracomeres1-4; head with mov- to a depth of 400 m; Nebaliopsistypica is bathypelagic. able,articulated rostrum; thoracopods1-5 uniramous Most speciesseem to occur in low- environ- and subchelate,second pair massiveand raptorial (all ments.One species,Dahlella caldariensis, is associated five are sometimescalled "maxillipeds" or gnathopods with the hydrothermal vents of the Galapagosand becausethey are involved in feeding); thoracopods the EastPacific Rise.Speonebalia cannoni is known only 6-8 biramous, ambulatory;pleopods biramous, with from marine caves. dendrobranchiate-likegills on exopods;antennules tri- Most leptostracanssuspension feed by stirring up ramous;antennae biramous, with large,paired, stalked bottom sediments.They are also capableof grasping compound eyes that are unique in the animal kingdom relatively large bits of food directly with the mandi- (Figures21.7 A-C, 21.27D,and 21.33K). bles.Some are carnivorousscavengers, and someare All500 or so living hoplocarids are placed in the known to aggregatein areason the seafloor where order Stomatopoda,known as mantis shrimps. They large amounts of detritus accumulate.In many species are relatively large crustaceans,ranging in length from the antennaeor antennulesof malesare modified to 2 to 30 cm. Compared with that of most malacostra- hold femalesduring copulation. cans,the muscle-filledabdomen is notably robust. 776 Chaoter Twentv-One

Most stomatopods are found in shallow tropical or and extant membersof the order (e.g., subtropical marine environments. Nearly all of them Anaspides),it has been suggestedthat syncaridsmay live inburrows excavated in soft sediments or in cracks encompassthe most primitive living eumalacostra- and crevices, among rubble, or in other protected can body plan. Bathynellaceansoccur worldwide spots. All species are raptorial carnivores, preying on in interstitial or groundwater habitats, whereasthe fishes, molluscs, cnidarians, and other crustaceans. The anaspididaceansare strictly Gondwanan in distribu- large, distinctive sirbchelae of the second thoracopods tion. Many Anaspidaceaare endemic to Tasmania, act either as crushers or as spears (Figure 21.7C). where they inhabit freshwater environments, such as Stomatopods crawl about using the posterior thora- open lake surfaces,streams, ponds, and crayfish bur- copods and the flaplike pleopods. They also can swim rows. No syncarids are marine. Thesereclusive eum- by metachronal beating of the pleopods (the swimmer- alacostracansshow various degreesof what somehave ets). For these relatively large animals, living in narrow regarded as paedomorphism, including small size burrows requires a high degree of maneuverability. (Anaspididaeincludes members to 5 cm, whereasmost The short carapace and the flexible, muscular abdomen othersare lessthan 1 cm long), eyelessness,and reduc- allow these animals to twist double and turn around tion or lossof pleopodsand someposterior pereopods. within their tunnels or in other cramped quarters. This Bathynellaceansare small (1-3 mm long), possess6 or ability facilitates an escape reaction whereby a mantis 7 pafusof long, thin swimming legs, and have a pleo- shrimp darts into its burrow rapidly head first, then telson formed by the fusion of the telson to the last turns around to face the entrance. pleonite. Stomatopods are one of orLly two groups of malacos- Syncarids either crawl or swim. Little is known tracans that possess pleopodal . Only the isopods about the biology of most species,although some are share this trait, but the pleopods are quite different in considered omnivorous. Unlike most other crusta- the two groups. The tubular, thin, highly branched gills ceans,which carry the eggsand developing early em- of stomatopods provide a large surface area for gas ex- bryos, syncarids lay their eggs or shed them into the change in these active animals. water following copulation.

Subclass Eumalacostraca Superorder Telsonwithout caudal rami; Head, thorax, and abdomen of 6-8-6 somites respec- 0,1.,or 3 pairs of maxillipeds; carapacepresent, cov- tively (plus telson); with 0, 7,2, or 3 thoracomeres fused ering and fused dorsally with head and entire thorax; with head, their respective appendages usually modi- usually with stalked compound eyes;gills thoracic. fied as maxillipeds; antennules and antennae primi- Although members of this group are highly diverse, tively biramous (but often reduced to uniramous); they are united by the presenceof a completecarapace antennae often with scalelike exopod; most with well that is fused with all thoracicsegments, forming a char- developed carapace, secondarily reduced in slmcarids acteristiccephalothorax. Most species(several thou- and some peracarids; gills primitively as thoracic epi- sand) belong to the order Decapoda.The other two pods; tail fan composed of telson plus paired uropods; orders are the Euphausiacea(krill), and the monotypic abdomen long and muscular. Three superorders: S1m- Amphionidacea. carida, Eucarida, and Peracarida. Order Euphausiacea Euphausidsare distinguished Superorder Without maxillipeds (Bathy- among the eucaridsby the absenceof maxillipeds, the nellacea) or with one pair of maxillipeds (Anaspid- exposureof the thoracic gills external to the carapace, acea); no carapacei pleon bears telson with or with- and the possessionof biramous pereopods(the last 1 or out furcal lobes; at least some thoracopods biramous, 2pairs sometimesbeing reduced).They are shrimplike eighth often reduced; pleopods variable; compound in appearance.Adults have antennal glands. Most of eyes present (stalked or sessile) or absent (Figure them have photophores on the eyestalks,the basesof 21,.7D,E).There are about 285 described species of s;m- the secondand sevenththoracopods, and between the carids in two orders, Anaspidacea and Bathlnellacea.a first 4 pairs of abdominal limbs. To many workers, the syncarids represent a key group The 90 or so speciesof euphausidsare allpelagic and in eumalacostracan evolution, and they may rep- rangein length from 4 to 15cm. The pleopods function resent an ancient relictual taxon that now inhabits as swimmerets.Euphausids are known from all ocean- refugial habitats. Through studies of the fossil record ic environmentsto depths of 5,000m. Most speciesare distinctly gregarious,and speciesthat occur in huge schools(krill) provide a major sourceof food for larger 4Until recently a third slmcarid order was recognized, the nektonic animals (baleenwhales, , fishes) and Stygocaridacea, endemic to the Southern Hemisphere. Most work- ers now agree that the stygocarids should be reduced to the rank evensome marine birds. Krill densities,particularly for of family within the order Anaspidacea. Euphausiasuperba, often exceed1,000 animals/m3 (6t+ PHYLUMARTHROPODA Crustacea: Crabs, Shrimps, and TheirKin 777

(A) Carapace Compound eye

Antennule

Pereopod Branchial I epipod Pleopod Photophore Antenna

Carapace

Antennule

Propodus

Fifth pleopod Maxilliped First pleopod

Figure 21 .8 Anatomy in the class Malacostraca, super- order Eucarida-euphausids and amphionidaceans. (A) General body form of the euphausid, Meganyctiphanes. (B) Pereopod of Euphausia superba. (C) reynaudii (female), the only living species of the Amphionidacea. first pair in femalesis uniramous and greatly enlarged, perhaps functioning to form a extend- g wet weight/m3).s Generally,euphausids are suspen- ing under the thorax. Femaleshave a reduced gut and sion feeders,although and detritivory also apparently do not feed.Amphionides is a worldwide occff (Figures21.8,4',8 arrd2L.2lB). member of marine oceanicplankton and occursto a depth of 1.,700m (Figure21.8C). Order Amphionidacea The singleknown speciesof the order Amphionid acea,Amphionides reynaudii, p os- Order Decapoda The decapodsare among the most sessesan enlargedcephalothorax covered by a thin, familiar eumalacostracans.They possessa well devel- almost membranous carapacethat extends to enclose oped carapaceenclosing a branchial chamber,but they the thoracopods.The thoracopods are biramous with differ from other eucarid ordersin always possessing3 short exopods. The first pair is modified as maxil- pairs of maxillipeds,leaving 5 pairs of functional unira- lipeds, and the last pair is absentin females.Some of mous or weaklybiramous pereopods(hence the name, the mouthparts are highly reduced in females.The Decapoda);one (or more) pairs of anteriorpereopods pleopods are biramous and natatory,except that the are usually clawed (chelate).Adults have antennal glands.Rearrangement of the subtaxawithin this order sWhere krill densities exceed about 100 grams per cubic meter, is a popular carcinologicalpastime (seeMartin and they are often fished commercially. Krill schools can extend for Davis 2001for an entry into the vast literature on deca- tens of miles, contain millions of tons of krill, and stain the ocean pod classification).In vernacularterms, nearly every red with their surface swarms in coastal waters. Large baleen whales can eat a ton of krill in one mouth-ful. Seals, fish, , decapodmay be recognizedas some sort of shrimp, and humans also eat krill. Krill fishine has been banned in most crab,lobster, or crayfish. of North America, but it continues inJapan where tens of thou- We do not want to belabor the issue of decapodgill sands of tons are landed annually and used mainly as feed for farmed fish. The largest krill is in the ocean surrounding nomenclature. However, the gills play a prominent role Antarctica, where they have been harvested commercially since in the of this group; thus, we provide brief the 1970s. In the 1980s, large fleets from the Soviet Union caught descriptionsof the basic types. All decapod gills arise up to 400,000 tons of annuallv, but the current citch is now down to about 120,000 tons (taken by Japan, Korea, as thoracic coxal exites(epipods), but their final place- Norway, Poland, the Ukraine, and the U.S.). ment varies. Thosethat remain attachedto the coxaeare 778 Chaoter Twentv-One podobranchs (= "foot gills"), but others eventually be- Suborder This group includes come associated with the articular membrane between over 500 species of decapods, most of which are the coxae and body and are thus called arthrobranchs (= penaeid and sergestid shrimps. As the name indicates, 'Joint gills"). Some actually end up on the lateral body these decapods possess dendrobranchiate gills (Figure wall, or side-surface of the thorax, as pleurobranchs 21,.288),a unique synapomorphy of the taxon. One (= "side gills"). The sequenceby which some of these genus/ Lucifer, has secondarily lost the gills completely. gills arise ontogdnetically varies. For example, in the The dendrobranchiate shrimps are further character- Dendrobranchiata and the , arthrobranchs izedby chelae on the first three pereopods, copula- appear before pleurobranchs, whereas in members of tory organs modified from the first pair of pleopods the Caridea the reverse is true. In most of the other deca- in males, and ventral expansions of the abdominal ter- pods the arthrobranchs and pleurobranchs tend to ap- gites (called pleural lobes). Generally, none of the che- pear simultaneously. These developmental differences lipeds is greatly enlarged. In addition, females of this may be minor heterochronic dissimilarities and of less group do not brood their eggs. Fertilization is external, phylogenetic importance than actual gill anatomy. and the embryos hatch as nauplius larvae (see the sec- Among the decapods, the gills can also be one of tion on Reproduction and Development later in this three basic structural types, described as dendrobran- chapter). Many of these animals are quite large, over chiate, trichobranchiate, and phyllobranchiate (Figure 30 cm long. The sergestids are pelagic and all marine, 21.28F.-D). All three of these gill types include a main whereas the penaeids are pelagic or benthic, and some axis carrying afferent and efferent blood vessels,but occur in brackish water. Some dendrobranchiates they differ markedly in the nature of the side filaments (e.9., Penaeus,Sergestes, , Sicyonia) are of major or branches. Dendrobranchiate gills bear two principal commercial importance in the world's shrimp fisher- branches off the main axis, each of which is divided ies, most of which are now being exploited beyond into multiple secondary branches. Trichobranchiate sustainable levels and often with fishing techniques gills bear a series of radiating unbranched tubular fila- that are highly habitat-destructive (Figures 27.9Aand ments. Phyllobranchiate gills are characterizedby a 2r.33G). double series of platelike or leaflike branches from the axis. Within each gill type, there may be considerable Suborder All of the remaining deca- variation. The occurrences of these three major gill pods belong to the suborder Pleocyemata. Members types among various taxa are presented below. of this taxon never possess dendrobranchiate gills. Close inspection of the proximal parts of the pe- The embryos are brooded on the female's pleopods reopods usually reveals another decapod feature: in and hatch at some stage later than the nauplius most forms, the basis and ischium are fused (as a basi- larva. Included in this suborder are several kinds of ischium), with the point of fusion often indicated by a shrimps, the crabs, crayfish, lobsters, and a host of suture line. Tegumental glands are also a ubiquitous less familiar forms. Most current workers now rec- feature among the Decapoda. These glands originate ognize 11 infraorders within the Pleocyemata, as we below the epidermal cells and produce a fluid that have done below, but a number of other schemes have opens on the surface of the cuticle. They have been been proposed and persist in the literature. One older reported from gills, legs, pleopods, and uropods. The approach divided decapods into two large groups, roles of tegmental glands are not well known, and they called the and Reptantia-the swimming have been suspected to be involved in cuticular tan- and walking decapods, respectively. Although these ning, the production of mucus by the mouthparts, the terms have largely been abandoned as formal taxa, production of cement substance involved with egg at- they still serve a useful descriptive purpose, and one tachment, and possibly also grooming. continues to see references to natant decapods and The 18,000or so living species of decapods comprise reptant decapods. a highly diverse group. They occur in all aquatic envi- ronments at all depths, and a few spend most of their Infraorder The procarids consist of a sin- lives on land. Many are pelagic, butbthers have adopt- gle family containing two genera of shrimp, Procaris and ed benthic sedentary, errant, or burrowing lifestyles. Vetericaris,that have been called "primitive shrimps." Decorating of the is frequently seen among Like caridean shrimp (below) and most other pleocye- the decapods, especially in spider crabs (Brachyura: mates, they bear flattened, platelike (nondendrobranch) ), which use Velcro-like hooked setae to at- gills, but they lack claws on any of their legs, have a very tach dead or living plants and animals; decorating has leglike (pediform) third maxilliped, and have epipods been shown to reduce predation through camouflage on all of the maxillipeds and pereopods, assumed to be and/ or chemical deterrence. Decapod feeding strate- an ancestral condition because most decapod groups no gies include suspension feeding, predation, herbivory, longer bear the full complement. Th"y are known from scavenging, and more. Most workers recognize two anchialine habitats-inland pools with connections to suborders: Dendrobranchiata and Pleocvemata. the sea (Figure 21.98). PHYLUM ARTHROPODA Crustacea:Crabs, Shrimps,and TheirKin 779

(B) Compound Secondpleomere

Antennule Antenna

Antennal scale Third maxillipeds

Pereopods----J Pleopods

Figure 21 .9 External anatomy and diver- sity in shrimps (Decapoda). (A) A penaeid shrimp (Dendrobranchiata), Penaeus seflferus. (B) A procarid shrimp (Procarididea), Procaris ascenslonis. (C) A hippo- lytid sh rimp (Caridea, ), Lysmata califo rn ica. (D)An alpheid, or snapping shrimp (Caridea,), Alpheus. (E) A stenopodid shrimp (Stenopodidea), Stenopus.

InfraorderCaridea The nearly3,500living species in associatedwith shallow benthic environments, espe- this infraorder are generallyreferred to as the caridean cially with coral reefs;others are known from the deep shrimps. Theseswimming decapodshave phyllobran- sea.Many are commensal,and the group includes chiate gills. The first 1 or 2 pairs of pereopodsare che- the cleanershrimps (e.g.,Stenopas) of tropical reefs, late and variably enlarged.The secondabdominal pleu- which are known to remove parasitesfrom local fish- ra (side walls) are distinctly enlarged to overlap both es.Stenopodids often occur as male-femalecouples. the first and third pleura. The first pleopods are gener- Perhapsthe most noted example of this bonding is ally somewhatreduced, but not much modified, in the associatedwith the glasssponge (Euplectella) shrimp, males(Figures 21.1K, 21.9C,D,2L24D, and 21.31D). Spongicolaaenusta. A young male and femaleshrimp enter the atrium of a host ,eventually growing InfraorderStenopodidea The 70or so speciesin this too large to escapeand thus spending the rest of their infraorder belong to three families. The first 3 pairs of days together. pereopodsare chelate,and the third pair is significant- ly larger than the others.The gills are trichobranchiate. Infraorder Brachyura Theseare the so-called"true The first pleopodsare uniramous in malesand females, crabs." The abdomen is symmetrical but highly but are not strikingly modified. The secondabdomi- reduced and flexed beneath the thorax, and uropods nal pleura are not expandedas they are in carideans are usually absent.The body, hidden beneatha well- (Figures2L.9E and 27.318). developed carapace,is distinctly flattened dorso- Thesecolorful shrimps are usually only a few cen- ventrally and often expandedlaterally. The gills are timeterslong (2-7 cm). Most speciesare tropical and typically phyllobranchiate, but exceptionsoccur. 780 ChapterTwenty-One

(A) Figure 21 .10 Anatomy and diversity of the "true," or brachy- (Decapoda: Compound uran, crabs Brachyura). (A,B) General crab anatomy: Palp of maxilliped Antennule eye frontal and ventral views of a swimming crab (family ). Antenna (C) A spider crab (family Majidae), Loxorhynchus. (D) A kelp crab Carapace Carpus /orat (Majidae), Pugettia. (E) An arrow crab (Majidae), Stenorhynchus. (F) A cancer crab (family Cancridae), Cancer. (G) A grapsid crab (family Grapsidae), Pachygrapsus. (H) A pinnotherid or crab (family ), Parapinnixa. (l) A xanthid crab (family ), Trapezia. Many members of this genus are obligate commensals in scleractinian corals. (J) A dromiid crab (fam- Third maxilliped ily Dromiidae), Hypoconcha (anterior view). Members of the Dromiidae carry bivalve mollusc shells (or other objects) on their backs. (K) A calappid crab (family Calappidae), Hepatus (ante- rior view). (L) Ventral views of a female (upper photo) and (lower photo) male Hemigrapsus sexdentatus.

(c) Claw of cheliped

Basi-ischium

Propodus

Dactyl

Carpus Coxa Thoracic sterna Merus Basis Abdomen Fifth pereopod PHYLUMARTHROPODA Crustacea: Crabs, Shrimps, and TheirKin 781

about a dozen families) all have direct development, incubate their embryos,and are independent of sea water. Some freshwater crabs are intermediate hosts of Paragonimus,a cosmotropicalparasitic human fluke, and others are obligate phoretic hosts of larval black flies (Simulium),the vector for Onchocercaaolaulus (the causativeagent of river blindness). A number of speciescarry other invertebrateson their carapace(e.g., ,) or on their claws (e.g.,anemones); these associationsare generally thought to be mutu- alistic, (K) providing camouflage or predator deterrence for the crab while their partner is moved about in the environment and may feed off debris from their host's feeding activities. The opener photo for this chapter shows the tropical Pacific teddy-bear crab,Polydectus cupulifer,which is densely coveredwith setaeand fre- quently carries a seaanemone on each cheliped. In the northeast Pacific, megalopaeand juveniles of the crabCancer gracilis ride (and feed) on the bell of cer- tain ; individuals of Phacellophoracamtschatica (Scyphozoa)have been found with hundreds of C. gra- ciils megalopae.There are about 7,000described spe- ciesof Brachyura.

Infraorder Anomura This group includes hermit crabs, galatheid crabs, king crabs,porcelain crabs, mole crabs, and sand crabs. The abdomen may be soft and asymmetrically twisted (as in hermit crabs) or symmetrical, short, and flexed beneath the thorax (as in porcelain crabs and others).Those with twisted abdomenstypically inhabit gastropod shells or other empty "houses" not of their own making. King crabs (Lithodidae and Hapalogastridae)probably evolved out of hermit crab-like ancestors.Carapace shape and gill structure vary. The first pereopodsare che- late; the third pereopodsare never chelate.The sec- ond, fourth, and fifth pairs are usually simple, but occasionallythey are chelateor subchelate.The fifth pereopods (and sometimes the fourth) are generally much reduced and do not function as walking limbs; the fifth pereopodsfunction as gill cleanersand often The first pereopods are chelateand usually enlarged. are not visible externally.The pleopods are reduced or Pereopods2 to 5 are typically simple, stenopodous absent.The eyes are positioned medial to the anten- walking legs,although in somegroups/ the fifth pereo- nae. The zoealarva is similar to that of the true crabs pods are also chelate.The eyesare positioned lateral to but is typically longer than broad, with the rostral the antennae.Males lack pleopods 3 to 5. The distinc- spine directed anteriorly.Most anomuransare marine, tive larval stageis called a zoea;its carapaceis spheri- but a few freshwater and semi-terrestrial speciesare cal and bears a ventrally directed rostral spine (or no known. The so-called"yeti crab" (Kiwahiisuta) was spine ) (Figure s 21.18, 21.10,21,.27H, 2L.28F,G, 21..29 C, discovered in 2005 from2,200 m-deep hydrothermal 21.32,and21,.33H,I). vents south of EasterIsland. It is remarkable for its Brachyuran crabs are mostly marine, but freshwa- " gatden" of filamentous bacteria that grow on the long ter, semi-terrestrial,and moist terrestrial speciesoccur setaeof the exoskeleton;the bacteriaare heterotrophic, in the tropics. The land crabs (certain speciesin the utilizing sulfides in the deep environment (the pre- families Gecarcinidae,, Grapsidae, etc.) ciserole of the bacteria,of severalspecies, in the life are still dependent on the oceanfor breeding and lar- history of the yeti crab is not yet well understood). A val development. The surprisingly large number of secondspecies of Kiwa was describedin 2011(Figures freshwatercrabs (about 3,000species, classified into 21.IF -L 2L.11C-G,21.24 A-C, 21.3IA, and 21. 33I). 782 ChapterTwenty-One

(A) CepholothoraVcarapace Major cheliped

Walking legs

Antenna Antennule

Cheliped. | | (Pereopod1)-. Lpereooods r-5 I

'::--:\-l- i:-;:t-l:-L- t. :) rfuP\,\ v_\L--ri-v

_--t 2 -J L Figure 21 .11 External anatomy and diversity in some other reptant decapods (Eumalacostraca, Eucarida). (A) A mud shrimp, Callianassa (). (B) A spiny lob- ster, Panulirus (Achelata). (C) A hermit crab, Paguristes, in its shell (Anomura). (D) A hermit crab, Pagurus, removed from its shell to expose the soft abdomen. (E) A porcelain crab, Petrolisthes (Anomura), with the reduced posterior pereopods extended. (F) A sand crab, Emerita (Anomura). umbrellacrab Cryptolithodes (Anomura), in ventral Infraorder Astacidea The 650+ species of crayfish l?Jl" and clawed lobsters comprise some of the most famil- iar decapods (Figure 21.2).As in most other decapods, the dorsoventrally flattened abdomen terminates in a of crayfish occur in North America alone, where they strong tail fan. The gills are trichobranchiate. The first 3 show high levels of endemicity to particular regionsor pairs of pereopods are always chelate, and the first pair river drainages.(Figures 21.27E,G and 21.298). is greatly enlarged. Homarus americanus,the American or Maine lobster, is strictly marine and is the largest liv- Infraorder Achelata This group includes the coral ing crustacean by weight (the record weight being over and spiny lobsters (family Palinuridae) and slipper 20 kilograms). Most crayfish live in fresh water, but a lobsters(family Scyllaridae).The nameAchelata comes few species live in damp soif where they may excavate from the fact that they lack chelaeon all pereopods as extensive and complex burrow systems. The 600+ spe- adults (exceptfor a small grooming claw on pereo- cies of freshwater crayfish comprise a monophyletic pod 5 in some females).The flattened abdomen bears group that is sister to clawed lobsters. Over 425 species atailfan; the carapacemay be cylindrical or flattened PHYLUMARTHROPODA Crustacea: Crabs, Shrimps, and TheirKin 789

dorsoventrally; the gills are trichobranchiate. The large, prejuvenile stagelacking the last pair of thoracopods flattened larvae, called phyllosomas becauseof their (no free-living larvae occur in this group) (Figures leaf{ike appearance,are unique and distinctive. All 21.72-21.15). speciesare marine, and they are found in a variety of The roughly 25,000species ofperacarids are divided habitats throughout the tropics.Ma.y speciesproduce among nine orders. The peracarids are an extremely soundsby rubbinga process(the plectrum) at the base successfulgroup of malacostracancrustaceans and of the antennae against i, "file" on the head (Figures are known from many habitats. Although most are 21.1M,21.11B, 21.30 A,C, and 21.33L). marine, many also occur on land and in fresh water, and severalspecies live in hot springs at temperatures Infraorders Gebiidea and Axiidea Thesetwo infra- of 30-50'C. Aquatic forms include planktonic as well orders, traditionally referred to collectively as the asbenthic speciesat all depths.The group includes the ,have recentlybeen recognizedas dis- most successfulterrestrial crustaceans-the pillbugs tinct. The vernacular term "thalassinid" is still some- and sowbugs of the order -and a few amphi- times used to refer to them together.The mud and pods that have invaded land and live in damp forest ghost shrimps are particularly difficult to placewithin leaf litter or gardens.Peracarids range in sizefrom tiny the decapods.Sometimes they are depicted as related interstitial forms only a few millimeters long to plank- to the crayfish and chelatelobsters (Astacidea), and tonic amphipods over 12 cm long (Cystisoma),deepsea sometimesthey are grouped with the hermit crabs necrophagousamphipods exceeding34 cm (Alicellagi- and their relatives (Anomura). Thesedecapods have a gantea),and benthic isopodsgrowing to 50 cm in length symmetrical abdomen that is flattened dorsoventrally (Bathynomusgiganteus). These animals exhibit all sorts and extendsposteriorly as a well-developedtailfan. of feeding strategies;a number of them, especiallyiso- The carapaceis somewhatcompressed laterally, and pods and amphipods,are commensalsor parasites. the gills are trichobranchiate.The first 2pairs of pereo- pods are chelate,and the first pair is generally much Order Mysida Carapacewell developed,covering enlarged.Most of theseanimals are marine burrowers most of thorax, but never fused with more than four or live in coral rubble. They generallyhave a rather anterior thoracic segments;maxillipeds (1-2 pairs) not thin, lightly sclerotizedcuticle, but some (e.g.,mem- associatedwith cephalic appendages;thoracomere bers of the family ) have thicker skeletonsand 1 separatedfrom head by internal skeletalbar; abdo- are more lobster-like in appearance.Gebiideans (par- men with well developed tail fan; pereopods bira- ticularly Upogebia,Callinnassa, and relatedgenera) often mous/ except last pair, which are sometimesreduced; occur in huge colonies on tidal flats, where their bur- pleopodsreduced or, in males,modified; compound row holes form characteristicpatterns on the sediment eyesstalked, sometimesreduced; gills absent;usually surface(Figures 21.1L and 21,.11,A). with a statocystin eachuropodal endopod; adults with antennalglands (Figures21.72A,8,21.308, and 21.33C). lnfraordersGlypheidea and The gly- There are more than 1,050species of mysids, rang- pheids are something of a relict group, representedby ing in length from about 2 mm to 8 cm. Most swim by two living genera (Neoglypheaand Laurentaglyphea), action of the thoracic exopods.Mysids are shrimplike each with a single species,of a formerly diverse crustaceansthat are often confused with the superfi- group known from the fossil record.Polychelids are cially similar euphausids(which lack oostegitei and a small group of blind deep-sealobsters, notable for uropodal statocysts).Mysids are pelagic or demer- having chelae on all of their pereopods and unusual, sal and are known from all oceandepths; a few spe- large, globatelarvae (called eryoneicuslarvae) unique cies occur in freshwater.Some species are intertidal among the decapods. and burrow in the sand during low . Most are omnivorous suspensionfeeders, eating algae,zoo- Superorder Peracarida Telsonwithout caudal planktorg and suspendeddetritus. In the past, mysids rami; 1 (rarely 2-3) pair of maxillipeds; maxilliped were combined with lophogastrids and the extinct basistypically produced into an anteriorly directed, Pygocephalomorphaas the "." bladelike endite; mandibles with articulated acces- sory processesin adults, between molar and incisor Order Similar to mysids, exceptfor processes/called the lacinia mobilis; carapace,when the following: maxillipeds (1 pair) are associated^with present, not fused with posterior pereonitesand usu- the cephalic appendages;thoracomere 1 not separat- ally reduced insize; gills thoracic or abdominal; with ed from head by internal skeletalbar; pleopods well unique, thinly flattened thoracic coxal endites, called developed; gills present;adults with both antennal oostegites,that form a ventral brood pouch or mar- and maxillary glands;without statocysts;all 7 pairs of supium in femalesall speciesexcept members of the pereopodswell developed and similar (exceptamong order (the latter using the cara- members of the family , in which their paceto brood embryos);young hatch as mancas,a structure varies) (Figures 21.I2C,D and 21.21G). 784 Chapter Twenty-One

(B) Compound Carapace

Antennule

Antennal scale Antenna Mandible Pleopods (c) Statocyst Pereopods Roshum Antennule Telson Uropod Coxa

Mandible Exopod

Endopod

Antenna Pereopods

Antennule \ / -Pseudorostrum

Figure 21 .12 Anatomy and diversity in some peracarid crus- taceans (Eumalacostraca; Peracarida)-mysids, lophogastrids, cumaceans, and tanaids. (A) A mysid, Bowmanella braziliensis. (B) Anatomy of a generalized mysid (Mysida). (C) Anatomy of a lophogastrid, Gnathophausla. (D) Second pereopod of Gnatho- phausia. (E) A cumacean, Diastylis, in its typical partially buried position. The arrows indicate the feeding and ventilation current. (F) A cumacean. (G) A tanaid. (H) Anatomy of a generalized tanaid. (H)

Antennule

Antenna Pleopods Gnathopod Pereopods (secondthoracopods) PHYLUMARTHROPODA Crustacea: Crabs, Shrimps, and TheirKin 785

There are about 60 known speciesof lophogastrids, two speciesof unusual crustaceansMictocaris halope most of which are 1-8 cm long, although the $antGnatho- (from marine cavesin Bermuda) and Hirsutia bathya- phausiaingens reaches 35 cm. All arepelagic swinuners, lls (from a benthic sample 1,000m deep in the Guyana and the group has a cosmopolitanoceanic distribution. Basin off northeasternSouth America). A third spe- Lophogastridsare primarily predatorson . ciesof Mictaceawas describedin 1988from Australia, and a fourth from the Bahamasrn7992; there are now Order Cumacea Carapacepresen! coveringand fused 6 speciesknown. Mictaceansare small,2-3.5 mm in to first three thoracic segments,whose appendagesare length.Mictocaris halope is the best known of thesespe- modified as maxillipeds, the first with modified bran- ciesbecause many specimenshave beenrecovered and chial apparatusassociated withbranchial cavity formed somehave been studied alive. It is pelagic in cavewa- by carapace;pereopods 1-5 ambulatory,simple, 1-4 ters and swims by using its pereopodal exopods.The may be biramous; pleopods usually absentin females statusof the Mictaceaas a monophyletic grouping and and present in males;telson sometimesfused with sixth its relationships to other peracarid orders is a subject pleonite, forming pleotelson;uropods styliform; com- of ongoing debate.Some workers recognize the fam- pound eyesabsent, or sessileand usually fused (Figures ily Hirsutiidae (containingHirsutia, Montucaris, and 21.7Pand21.12E,F). Thetispelecaris)as a separateorder, the Bochusacea Cumaceansare small, odd{ooking crustaceanswith (malepleopods biramous). a large,bulbous anterior end and a long, slenderposte- rior-resembling horizontal commas!The great carcin- Order Carapaceshort, fused with ologist Waldo Schmitt referred to them as "little won- first thoracomere;1 pair of maxillipeds; pereopods1-Z ders and queer blunders." They occur worldwide and simple,biramous, with shortenedexopods; exopods include about 1,500species, most of which arebetween on legs 1-3 modified for producing currents, on legs 0.1 and 2 cm long, though some speciesin cold water 4-7 as gills; pleopods 1-4 biramous, natatory; pleopod reach 3 cm in length. Most are marine, although a few 5 reduced;tail fan well developed; compound eyes brackish-waterspecies are known. They live in associa- nonfunctional or absen! but eyestalkspersist (Figures tion with bottom sediments,but are capableof swim- 21.13Aand 21.21H).The order Spelaeogriphaceais cur- ming and probably leavethe bottom to breed.Most are rently known from only four living species.These rare, deposit feedersor predators on the meiofauna,others small (lessthan 1 cm) peracaridswere long known eat the organic film on sand grains. only from a single speciesliving in a freshwater stream in Cave on TableMountain, South Africa. A sec- Order Carapacepresent and fused with ond speciesis known from a freshwatercave in , first two thoracicsegments; thoracopods 1.-2 are maxil- and a third and fourth specieswere describedfrom an lipeds, the secondbeing chelate;thoracopods 3-8 are aquifer in Australia. Little is known about the biology simple, ambulatory pereopods;pleopods presentor of theseanimals, but they are suspectedto be detritus absent;uropods biramous or uniramous; telson and feeders.Like thermosbaenaceans,spelaeogriphaceans last one or two pleonites fused as pleotelson;adults are thought to be relicts of a more widespreadshallow- with maxillary and (vestigial) antennal glands; com- water marine Tethyan fauna stranded in interstitial and pound eyes absent,or present and on cephalic lobes. ground-water environmentsduring periods of marine Membersof this order areknown worldwide from ben- regression. thic marine habitats; a few live in brackish or nearly fresh water.Most of the 1,500or so speciesare small, OrderThermosbaenacea Carapacepresent,fused ranging from 0.5 to 2 cm in length. They often live in with first thoracomereand extending back over 2-3 burrows or tubesand areknown from all oceandepths. additional segments;1 pair of maxillipeds; pereopods Many are suspensionfeeders, others are detritivores, biramous,simple, lacking epipods and oostegites;cara- and still others arepredators (Figure 21.12G,H). pace forms dorsal brood pouch (unlike all other pera- carids,which form the brood pouch from ventral ooste- Order Without a carapace,but with a well gites);2 pairs of uniramous pleopods;uropods bira- developed head shield fused with first thoracomere mous; telson free or forming pleotelson with last ple- and produced laterally over basesof mouthparts;1 pair onite; eyesabsent (Figure 21.138,C).About 34 species of maxillipeds; pereopodssimple, 1-5 or 2-6biramous, of thermosbaenaceansare recognizedin sevengenera. exopodsnatatory; gills absent;pleopods reduced,uni- Thermosbaenamirabilis is known from freshwaterhot ramous or biramous; uropods biramous, with 2-5 seg- springs in North Africa, where it lives at temperatures mented rami; telson not fused with pleonites; stalked in excessof 40'C. Severalspecies in other generaoccur eyespresent (Mictocaris) but lacking any evidenceof in much cooler fresh waters, typically in groundwater visual elements,or absent(Hirsutin) (Figure 21.13D-E). or in caves.Other speciesare marine or inhabit under- Mictaceais the most recently (1985)established per- ground anchialinepools. Limited data suggestthat acaridanorder. The order was erectedto accommodate thermosbaenaceansfeed on plant detritus. 786 Chapter Twenty-One Ocular lobe

(A) Antennule

Pereopods 1-7 Carapace

Pleopods (B) Thoracomeres3-8 Antennule

Pereopods1-7 Endopod

Pleopods

Antennule

Exopod Endopod

LPereopod 5r

Figure 21 .13 More peracarids. (4 The spelaeogriphacean, Spelaeogriphus. (B) The thermosbaenacean, Monodella. (C'1A thermosbaenacean. (D,E) The mictacean, Mictocaris.

pleopods biramous and well developed, natatory and Order lsopoda Carapaceabsent; first thoracomere for gas exchange (functioning as gills in aquatic taxa, fused with head; 1 pair of maxillipeds;7 pairs of uni- and with air sacs called pseudotrachea in most ter- ramous pereopods,the first of which is sometimes restrial Oniscidea);adults with maxillary and (ves- subchelate,others usually simple (gnathiidshave only tigial) antennal glands; telson fused with one to six five pairs of pereopods,as thoracopod2 is a maxilli- pleonites,forming pleotelson;eyes usually sessileand pedal "pylopod" and thoracopod8 is missing);pereo- compound, absentfrom some,pedunculate in most pods variable, modified as ambulatory, prehensile,or Gnathiidea;with biphasic molting (posterior region swimming; in the more derived suborderspereopodal molts before anterior region) (Figures 27.7Q,2L.L4, coxaeare expandedas lateral side plates (coxalplates); 2I.21I,2L.28H,I, and 21.33M). PHYLUMARTHROPODA Crustacea:Crabs, Shrimps, and TheirKin 787

Antennule (E Compound eye

Antenna

Pereonite one (= thoracomere two)

Coxal plates

(E) Pleotelson -l Protopod

Exopod UroPod Endopod _l

(G)

Figure 21 .14 More peracarids: members of the order lsopoda. (A) A flabelliferan, Excorallana (family ). (B) A fla- belliferan, Paracerceis (family ). Male mem- bers of this genus possess greatly enlarged uropods. (C) A flabelliferan, Codonophilus (family ). Members of this genus are parasites that attach to the tongues of various marine fishes. (D) A fla- The isopods comprise about 10,500marine, freshwa- belliferan, Heteroserolis (family Serolidae). (E) A valviferan, ldotea (tamily (F) ter, and terrestrial species, ranging in length from 0.5 to ldoteidae). An asellote, Joeropsis (tam- ily ). (G) An anthurid, Mesanthura (family 500 mm, the largest being species of the benthic genus ). (H) A gnathiidean, Gnathia (family ). Bathynomus(). They are common inhabit- Note the grossly enlarged mandibles characteristic of ants of nearly all environmenti, and some groups are male Gnathiidea. (l) An oniscidean, Ligia (the common exclusively (e.9., Bopyridae, Cymothoidae) or partly seashore "rock louse"). 788 Chapter TwentY-One (A)

Key $-ffi utoto-" ffi H"o.t ffi Coxalplates F,--II]P"."o" Antennule Gnathopods ! lleopads

Pereopods Anterrrule

Sessile (c) Lateral gili

Pereopod3 Medial gill

Pereopods

Figure 21 .15 And still more peracarids: amphipod diversity' (A) General anatomy of a gammaridean amphipod. (B) General anat- omy of a hyperiidean amphipod. (C) General anatomy of a cyamid amphipod (Cyamus monodontis). (D) A gammaridean, Melita' (E) A caprellid amphipod. (F) A cyamid amphipod, Cyamus erraticus, para- sitic on right whales. (G,H) Two gammaridean amphipods: (G) Hyale, a beach hopper, and (H) Heterophlias, an unusual, dorsoventrally flattened species. (l-K) Three hyperiidean amphipods: (l) Primno' (J) Leptocottis, and (K) a hyperiid on its host medusa' (L) A free-living caprellid, Capretta. (M) An ingolfiellid amphipod, lngolfiella' PHYLUMARTHROPODA Crustacea:Crabs, Shrimps,and Their Kin 789

(L)

(e.9.,Gnathiidae) parasitic. The suborderOniscidea in- Order Amphipoda Carapaceabsent; first thoraco- cludesabout 5,000species that have invaded land (pill- mere fused to head; 1,pair of maxillipeds; 7 pairs of bugs and sowbugs);they are the most successfulterres- uniramous pereopods,with first, second,and some- trial crustaceans.Their direct development, flattened times others frequently modified as chelae or sub- shape,osmoregulatory capabilities,thickened cuticle, chelae;pereopodal coxae expanded as lateral side and aerial gasexchange organs (pseudotrachea)allow plates (coxalplates); gills thoracic (medial pereopo- most oniscideansto live completely divorced from dal epipods);adults with antennalglands; abdomen aquatic environments. Fossilsas old as 325million "divided" into fwo regions of three segmentseach, an years ()have beenreported. anterior "pleon" and posterior urosome,with anterior Isopod feeding habits are extremely diverse. Many appendagesas typical pleopodsand urosomalappend- are herbivorous or omnivorous scavengers,but direct agesmodified asuropods; telson free or fused with last plant feeders,detritivores, and predatorsare also com- urosomite;other urosomitessometimes fused; com- mon. Some are parasites(e.g., on fishes or on other pound eyessessile, absent in some,huge in many (but crustaceans)that feed on the tissuefluids of their hosts. not all) members of the suborder (Figures Overall, grinding mandibles and herbivory seemto 21.1NO, 21.15,21.23, 21.27F, and 21.29D). represent the primitive state, with slicing or piercing Isopods and amphipods sharemany featuresand mandibles and predation appearing later in the evolu- are often said to be closely related. Earlier workers tion of severalisopod clades. recognizedthese similarities (e.g.,sessile compound 790 Chapter Twenty-One eyes, loss of carapace, and presence of coxal plates) contains only about 40 species, most of which live in and classified them together as the "Edriopthalma" subterranean fresh and brackish waters, although a few or "Acarida." Flowever, recent work suggests that are marine and interstitial. Little is known about their many similarities between these two taxa may be con- biology. The 300 or so species of caprellid amphipods vergences or parallelisms. The roughly 11,000species ("skeleton shrimp") are highly modified for clinging to of amphipods range inlength from tiny 1mm forms other organisms, including filamentous algae and hy- to giant deep-sea'benthic speciesreaching 29 cm, and droids. In most speciesthe body and appendages are a group of planktonic forms exceeds 10 cm. They very narrow and elongated. In one family of caprellids, have invaded most marine and freshwater habitats the Cyamidae (with 28 species),individuals are obligate and often constitute a large portion of the biomass in symbionts on cetaceans(whales, dolphins, and porpois- many areas. The largest known amphipod is Alicelkt es) and have flattened bodies and prehensile legs. gigantea, a cosmopolitan marine species living at In addition to , amphipods exhibit a vast depths up to 7,000m. array of feeding strategies, including scavenging, her- The principal suborder is Gammaridea. A few gam- bivory, carnivory, and suspension feeding. marideans are semiterrestrial in moist forest leaf litter or on supralittoral sandy beaches (e.9.,beach hop- "Maxillopodans" The following seven classes- pers); a few others live in moist gardens and green- Thecostraca, Tantulocarida, , , houses (e.g.,Talitrus sylaaticusand T. pncificus).They , Copepoda, and Ostracoda-histori- are common in subterranean groundwater ecosystems cally were united in a group called the of caves, the majority being stygobionts-obligatory that is now known to be artificial (nonmonophyletic). groundwater species characterized by reduction or loss Howeveq, many of these "maxillopodan" groups share of eyes, pigmentation, and occasionally appendages. some basic characteristics. These include a body of five About 900 species of stygobiontic amphipods have cephalic, six thoracic, and four abdominal somites, plus been described, including the diverse genercNiphargus a telson, but reductions of this basic 5-6-4body plan are (in Europe) and Stygobromus(in North America), each common, and different specialists sometimes interpret with over 100 described species. However, most of the the nature of these tagmata in different ways, leading gammaridean amphipods are marine benthic species, to some confusion. Additional characters that most of and a few have adopted a pelagic lifestyle, usually in these classeshave in common are: thoracomeres vari- deep oceanic waters. There are many intertidal spe- ously fused with cephalon; usually with caudal rami; cies, and a great many of these live in association with thoracic segments with biramous (sometimes unira- other invertebrates and with algae. Domicolous gam- mous) limbs,lacking epipods (except in many ostra- maridean amphipods in at least three families spin silk cods); abdominal segments lack typical appendages; from their legs that is used for consolidating the walls carapace present or reduced; with both simple and of their tube or shelter. compound eyes, the latter being unique, with three The suborder Hyperiidea includes exclusively pe- cups, each with tapetal cells (an affangement still often lagic amphipods that have apparently escaped the referred to as the maxillopodan eye). confines of benthic life by becoming associated with Most of these former "maxillopodans" are small other plankters, particularly gelatinous zooplankton crustaceans, barnacles being a notable exception. They such as medusae, ctenophores, and salps. The hype- are generally recognizable by their shortened bodies, riideans are usually characterized by huge eyes (and especially the reduced abdomen, and by the absence a few other inconsistent features), but several groups of a full complement of legs. The reductions in body bear eyes no larger than those of most gammarideans. size and leg number, emphasis on the naupliar eye, The Hyperiidea are almost certainly a polyphyletic minimal appendage specialization, and certain other group, and it is thought that several lineages are de- features have led biologists to hypothesize that pae- rived independently from various gammaridean an- domorphosis (progenesis) played a role in the origin cestors, although a modern phylogenetic analysis has of some of these classes.That is, in many ways, they yet to be attempted. The precise nature of the relation- resemble early postlarval forms that evolved sexual ships between hyperiideans and their zooplankton maturity before attaining all the adult features. Over hosts remains controversial. Some appear to eat host 26,000 species have been described within the seven tissue, others may kill the host to fashion a floating classes. "home," and still others may utilize the host merely for transport or as a nursery for newly hatched young. Class Thecostraca Specimens of the scyphozoarr Phacellophoracamtschtica This group includes the bamacles, parasitic ascothorac- have been found with nearly 500 Hyperia medusarum ids, and mysterious "y-lalae." The thecostracanclade riding (and feeding) on it. is defined by several rather subtle synapomorphies of There are two other small amphipod suborders: cuticular fine structure, including cephalic chemosen- and Caprellidea. The first suborder sory structures known as lattice organs. The group is PHYLUMARTHROPODA Crustacea: Crabs, Shrimps, and TheirKin 791

also supportedby molecularphylogenetic analyses. All crystalline cone structure in the compound eye, a fea- taxa have pelagic larvae, the terminal instar of which ture not known from any other crustaceangroup and possessesprehensile antennules and is specializedfor perhapsa vestigeof the ancestralthecostracan body locating and attaching to the substratum of the sessile plan. Most speciesof barnaclesare , adult state. whereasseparate are the rule in acrothoracicans and rhizocephalans,and someandrogonochoristic spe- Subclass Ascothiracidd About 125described spe- cies (males+ hermaphrodites;e.g., Scalpellum)have cies of parasitesof anthozoansand . alsobeen reported. Although greatly modified, they retain a bivalved Locomotion in barnaclesis generally confined to carapaceand the full complement of thoracic and the larval stages,although adults of a few speciesare abdominal segments(facts that suggestthey might be specifically adapted to live attached to floating ob- the most primitive living thecostracans).Ascothoracids jects (e.9.,, pumice, logs) or nektonic marine generally have mouthparts modified for piercing and animals (e.g.,whales, sea turtles). Others are often sucking body fluids, but some live inside other ani- found on the shells and exoskeletonsof various er- mals and absorbthe host's tissuefluids. In at least one rant invertebrates(e.9., crabs and gastropods),which species,Synagoga mira, malesretain the ability to swim inadvertently provide a meansof transportation from throughout their lives, attaching only temporarily one place to another.Thoracican and acrothoraci- while feeding on corals(Figure 21.16F). can barnaclesuse their feathery thoracopods (cirri) to suspensionfeed. Barnaclesin the family Coronulidae Subclass Cirripedia Primitively with tagmataas in are suspensionfeeders that attach to whales and tur- the class,but in most groups the adultbody is modified tles (e.g., , P latylep as, S t omat oI ep as, Cor onula, for sessileor parasitic life; thorax of six segmentswith Xenobqlanus).The 265 or so known speciesof rhizo- paired biramous appendages;abdomen without limbs; cephalansare all endoparasitic in other Crustacea, telson absentin most, although caudal rami persist on and are the most highly modified of all cirripedes. abdomen in some;nauplius larva with frontolateral They mainly inhabit decapodcrustaceans, but a few horns; unique, "bivalved" cypris larva; adult carapace are known from isopods/cumaceans, stomatopods, "bivalved" (folded) or forming fleshy mantle; first tho- and even thoracican barnacles.Some even parasitize racomereoften fused with cephalonand bearing max- freshwaterand terrestrialcrabs. The body consistsof illiped-like oral appendages;female gonopores near a reproductive part (the externa)positioned outside basesof first thoracic limbs, male gonoporeon median the host's body, and an internal, ramifying, nutrient- penis on last thoracicor first abdominal segment;com- absorbingpart (the interna).6 pound eyeslost in adults (Figures21.15,T,21.16A-E, 21.25,2L.26, 21..278,C, 21.32E, and 21.33F). Subcfass Monogeneric(Hansenocaris): The 1,285or so describedcirripede speciesare most- The "y-larvae," a half-dozen small (250-620mm) ly free-living barnacles,but this group also includes marine nauplii and cyprids (Figure 21.16I).Although some strange parasitic "barrlacles" rarely seenexcept known sinceHansen's original description in 1899,the by specialists.The common acorn and goosebarnacles adult stage of these animals has still not been identi- belong to the superorderThoracica. The superorder fied. However, a stage subsequentto the y-larva, the consistsof minute animals that burrow slug-like ypsigon stage,has been induced by treat- into calcareoussubstrata, including coralsand mollusc ing y-larvaewith molting hormones.The prehensile shells (Figure21.16G). The superorderRhizocephala antennulesand hooked labrum of the y-cyprids and are exceptionallymodified parasitesof other crusta- the degenerative nature of the ypsigon suggest that the ceans/especially decapods (Figure 21.16H). adults areparasitic in yet-to-be-identifiedhosts. If the body plan of the cirripedesis derived from something similar to what is seenin other "maxillopo- Class Tantulocarida dan" classes,then it has been so extensivelymodified Bizarceparasites of deep-watercrustaceans. juveniles that its basic features are nearly unrecognizablein with cephalon,6-segmentedthorax, and abdomenof adults of this subclass.The abdomenis greatly reduced up to7 segments;cephalon lacking appendages(other in adults, and also in most cypris larvae. In cyprids than antennulesin one known stageonly) but with an (cypris larvae) the carapaceis always present and "bi- internal median stylet; thoracopods1-5 biramous, 6 vaIved," the two sidesbeing held by a transversecypris adductor muscle; in adults the carapacemay be lost oRhizocephalans (Rhizocephala)or modified as a membranous,saclike of the family infest only decapod crustaceans and have been suggested as biological control agents mantle (thoracicansand acrothoracicans).In the bar- for invasive exotics such as the green crab (), nacles(Thoracica), it is this mantle that producesthe fa- which are upsetting coastal ecosystems worldwide. Sacculinds miliar calcareousplates that enclosethe body. have the ability to take control over such maior host functions Cyprids as molting and reproduction, and also to compromise the host's and adult acrothoracicansshare a unique tripartite lmmune system. 792 Chapter Twenty-One

(A) E

Mantle opening

Attached male

Maxilla PHYLUMARTHROPODA Crustacea:Crabs, Shrimps,and Their Kin 793

{ Figure 21 .16 Anatomy and diversity in the class The tiny tantulocaridsare lessthan 0.5 mm long. Thecostraca-barnacles and their kin. (A-E) Thoracican They attach to their hosts by penetrating the body with barnacles. (A) A sessile (acorn) barnacle with its cirri a protruding cephalic stylet. The young bear natatory extended for feeding. (B) Plate terminology in a balano- morph (acorn) barnacle. (C) The lepadomorph (stalked) thoracopods.About three dozen speciesin 22 genera barnacle Pollicipes polymerus. (D) Verruca, the "wart" bar- have been described(Figures 21.1V and 21.77).They nacle. (E) Two thorapican barnacles that live in association are known from abyssaldepths to the intertidal zone, with each other and'with whales. The stalked barnacle from polar to tropical waters, and from anchialhe pools Conchoderma attaches to the sessile barnacle Coronula, and hydrothermal vents, always as parasiteson other which in turn attaches to the skin of certain whales. (F) crustaceans.Until recently, members of this group had The ascothoracican Ascothorax ophiocentenis, a para- beenassigned to various parasitic site that feeds periodically on echinoderms (longitudinal groups of Copepoda section). (G) An acrothoracican, Alcippe. Note the highly and Cirripedia.In 1983Geoffrey Boxshall and Roger modified female and the tiny attached male. This species Lincoln proposed the new classTantulocarida. Some bores into calcareous substrata such as coral skeletons. early work on the group supported a view of these ani- (H) A crab (Carcinus) infected with the rhizocephalan mals asmaxillopodans, although the presenceof six or carcini. The crab's right side is shown as trans- sevenabdominal segmentsin juveniles of somespecies parent, exposing the ramifying body of the parasite. (l) A is inconsistent with this view; they are now believed to cypris y-larva, in lateral and dorsal views. be allied to the Thecostraca.The life rycle is unique and includes a larva called the tantulus.

uniramous; abdomenwithout appendagesbut with Class Branchiura caudalrami; adults highlymodified, with "unsegment- Body compact and oval, head and most of trunk cov- ed" sacciformthorax and a reduced abdomenbearing ered by broad carapace;antennules and antennaere- a uniramous penis on the first segment;female gono- duced, the latter sometimesabsent; mouthparts modi- pores on fifth thoracic segment. fied for parasitism;no maxillipeds; thorax reduced

Figure 21 .17 Anatomy in the class Tantulocarida. (A) An adult Basipodella atlantica. Note the absence of an abdomen and the modifications for parasitic life. (B) Basipodella attached to the antenna of a copepod host. (C,D) Microdajus pectinatus on a crustacean host, adult, and juvenile (SEM). 794 Chapter Twenty-One

(A)

Antennule

Antenna

Mandible

Maxillule Maxilla Maxilliped Third thoracic appendage

First abdominal segment

udal ramus

Figure 21 .18 Anatomy of the classes Mystacocarida, Copepoda, and Branchiura. (A) General anatomy and SEM of the mystacocarid Derocheilocaris. (B) General anatomy of Antennule a cyclopoid copepod. (C-E) General body forms of (C) a cala- noid, (D) a harpacticoid, and (E) a cyclopoid copepod. Note the points of body articulation (dark band) and the position of the genital segment (shaded segment). Roman numerals are thoracic segments; Arabic numerals are abdominal seg- ments; T = telson. (F) An elaborately setose calanoid copepod adapted for flotation. (G) A poecilostomatid copepod, Ergasilus pitalicus, ectoparasitic on cichlid fishes. (H) A female sipho- nostomatid copepod ( sp.) with egg sacs. (l) A female siphonostomatid copepod (Trebius heterodont, a parasite of horn in California) with egg sacs. (J) A siphonostomatid copepod, Clavella adunca, showing extreme body reduction; this species attaches to the gills of fishes by its elongate max- illae. (K) Notodelphys, a wormlike cyclopoid copepod adapted for endoparasitism in tunicates. (L) Argulus foliaceus, a branchiuran that parasitizes fishes. Note the powerful hooked suckers (modified maxillules) on the ventral surface.

midventral surfaceof last thoracic somite;paired, ses- to four segments, with paired biramous appendages; sile compound eyes and one to three median simple abdomen unsegmented, bilobed, limbless, but with eyes(Figure 21.18L). minute caudal rami; female gonopores at bases of The Branchiuracomprise about 230 speciesof ec- fourth thoracic legs, male with single gonopore on toparasiteson marine and freshwater fishes.The PHYLUMARTHROPODA Crustacea:Crabs, Shrimps,and Their Kin 795

Maxillule (hookedsucker)

First thoracic limb 796 Chapter Twenty-One

(A) (B)

Hooks Claw glands

Penehation stvlet

Figure 21 .19 Anatomy and diversity in the class Pentastomida. (A) Linguatula se rrata. (B) Cep hal obae n a tet rapod a. (C) lnternal anatomy of female Penta- stomum. (D) Internal anatomy of female Waddycephalus teretiusculus, a parasite of Australian snakes. (E) A generalized pentastomid primary larva.

antennules generally bear hooks or spines for attach- agesreduced to 2 pairs of head appendages,lobelike ment to their host fish. The mandibles are reduced and with chitinous claws used to cling to host. Body in size and complexity, bear cutting edges,and are cuticle nonchitinous and highly porous. Body muscles housed within a styliform "proboscis" apparatus.The somewhat sheetlike,but clearly segmentaland cross- maxillules are clawed in Dolops,but they are modi- striated. Mouth lacks jaws; often on end of snoutlike fied as stalked suckersin the other genera(Argulus, projection;connected to a muscular pumping pharlmx Chonopeltis,Dipteropeltis). The uniramous maxillae usu- used to suck blood from host. The combination of the ally bear attachmenthooks. The thoracopodsare bira- snout and the 2 pairs of legs gives the appearanceof mous and used for swimming when the animal is not there being five mouths, hencethe name (Greekpenta, attached to a host. Branchiurans feed by piercing the "fiye"; stomida,"mouths"). In many speciesthe ap- skin of their hosts and sucking blood or tissue fluids. pendagesare reduced to no more than the terminal Once they locate a host, they crawl toward the fish's claws. No specific gas exchange,circulatory, or excre- head and anchorin a spot where water flow turbulence tory organs.Gonochoristic; females larger than males. is low (e.g.,behind a fin or gill operculum). About 130described species, including two cosmopoli- Members of the genusArgulus occur worldwide, tan speciesthat can occasionallyinfest humans (Figure and can pose a seriousproblem to ,but 21,.1e). members of the other generahave restricted distribu- For yearsit was believedthat pentastomidswere al- tions. Chonopeltisis found only in Africa, Dipteropeltis lied with the fossil lobopodians, onychophorans,and in South America, and Dolopsin SouthAmerica, Africa, tardigradesas some kind of segmented,vermiform, and Tasmania. proto-arthropod creature-and some workers still entertain this idea. However, independent molecular Class Pentastomida studies suggestthe pentastomids are highly modified Obligatory parasites of various amphibians, reptiles, crustaceans,perhaps derived from the Branchiura. birds, and mammals. Adults inhabit respiratory tracts Corroboration has come from cladistic analysesof (, nasalpassages, etc.) of their hosts.Body highly sperm and larval morphology, anato- modified, wormlike, 2-73 cmin length. Adult append- my, and cuticular fine strucfure. PHYLUMARTHROPODA Crustacea: Crabs, Shrimps, and TheirKin 797

Work on the Swedish Orsten fauna indicates that There are more than 12,500 described species of pentastomid-like animals had appeared as early as . They can be incredibly abundant in the the late Cambrian (500 Ma), long before the land ver- world's seas,and also in some lakes-by one estimate, tebrates had evolved. \zVhatmight the original hosts of they outnumber all other multicellular forms of life these parasites have been? Conodont are com- on Earth. Most are small,0.5-10 mm long, but some mon in all the Cambrian localities that have yielded free-living forms exceed 1.5 cm in length, and certain pentastomids, raising the possibility that conodonts highly modified parasites may reach 25 cm. The bod- (also long a mystery, but now widely regarded as parts ies of most copepods are distinctly divided into three of early fishlike vertebrates) may have been at least one tagmata, the names of which vary among authors. of the original hosts of these early Pentastomida. The first region includes the five fused head segments and one or two additional fused thoracic somites; it Class Mystacocarida is called a cephalosome (= ggphrlothorax) and bears Body divided into cephalon and 1O-segmented trunk; the usual head appendages and maxillipeds. All of telson with clawlike caudal rami; cephalon character- the other limbs arise on the remaining thoracic seg- istically cleft; all cephalic appendages nearly identical, ments, which together constitute the metasome. The antennae and mandibles biramous; antennules, max- abdomen, or urosome, bears no limbs. The append- illules, and maxillae uniramous; first trunk segment age-bearing regions of the body (cephalosome and bears maxillipeds but is not fused with cephalon; no metasome) are frequently collectively called the pro- carapace; gonopores on fourth trunk segment; trunk some. The majority of the free-living copepods, and segments 2-5 with short, single-segment appendages those most frequently encountered, belong to the (Figure 21.i8A). orders , , and , There are only 13 described species of mystaco- although even some of these are parasitic. We focus carids, eight in the genus Derocheilocqrisand five in here on these three groups and then briefly discuss Ctenocheilocaris.Most are less than 0.5 mm long, al- some of the other, smaller orders and their modifica- though D. ingensreaches 1 mm. The head is marked by tions for parasitism. The calanoids are characterized a transverse "cephalic constriction" between the origins by a point of major body flexure between the meta- of the first and second anterurae, perhaps a remnant of some and the urosome, marked by a distinct nar- primitive head segmentation. In addition, the lack of fu- rowing of the body. They possess greatly elongate sion of the cephalon and maxillipedal tmnk segment the antennules. Most of the calanoids are planktonic, and simplicity of the mouth appendages, and other features as a group they are extremely important as primary have led some workers to propose that the mystacoca- consumers in freshwater and marine food webs. The rids are among the most primitive living crustaceans. point of body flexure in the orders Harpacticoida and These attributes may, however, simply be related to a Cyclopoida is between the last two (fifth and sixth) neotenic origin and specialization for interstitial habitats. metasomal segments. (Note: Some authors define Mystacocarids are marine, interstitial crustaceans the urosome in harpacticoids and cyclopoids as that that live in littoral and sublittoral sands throughout the region of the body posterior to this point of flexure.) world's temperate and subtropical seas.Their rather Harpacticoids are generally rather vermiform, with vermiform body and small size are clearly the posterior segments not much narrower than the to life among sand grains. Mystacocarids are thought anterior; cyclopoids generally narrow abruptly at the to feed by scraping organic material from the surfaces major body flexure. Both the antennules and the an- of sand grains with their setose mouthparts. tennae are quite short in harpacticoids, but the latter are moderately long in cyclopoids (although never Class Copepoda as long as the antennules of calanoids). The anten- Without a catapace, but with a well developed cephal- nae are uniramous in cyclopoids but biramous in the ic shield; single, median, simple maxillopodan eye other two groups. Most harpacticoids are benthic, (sometimes lacking); one or more thoracomeres fused and those that have adapted to a planktonic lifestyle to head; thorax of six segments, the first always fused show modified body shapes. Harpacticoids occur in to the head and with maxillipeds; abdomen of five seg- all aquatic environments; encystment is known to ments, including anal somite (= telson); well developed occur in at least a few freshwater and marine species. caudal rami; abdomen without appendages, except an Cyclopoids are known from fresh and salt water, and occasional reduced pair on the first segment, associ- most are planktonic. ated with the gonopores; point of main body flexure The nonparasitic copepods move by crawling or varies among major groupsi antennules uniramous, swimming, using some or all of the thoracic limbs. antennae uniramous or biramous ; 4-5 pafus of natatory Many of the planktonic forms have very setoseappend- thoracopods, most locked together for swimming; pos- ages, offering a high resistance to sinking. Calanoids terior thoracopods always biramous (Figures 27.7U, are predominantly planktonic feeders. Benthic harpac- 21.18B-K, 21.27A, 27.30D,and 21.33D). ticoids are often reported as detritus feeders, but many 798 Chapter Twentv-One feed predominantly on microorganisms living on the modified fifth limbs are in fact these appendages. The surface of detritus or sediment particles (e.g., , trunk seldom shows external evidence of segmenta- bacteria, and ). tion, although all 11 postcephalic somites are discern- Of the seven remaining orders, the Mormonilloida able in some taxa. The trunk limbs vary in structure are planktonic; the are known from among taxa and on individuals. The third pair of trunk deep-sea epibenthic habitats as well as anchialine caves limbs bears the gonopores and constitutes the so-called in both the Pacific and Atlantic; and the copulatory organ. are planktonic as adults, but the larval stages are en- Ostracods are one of the most successful groups of doparasites of certain gastropods, polychaetes, and crustaceans. They also have the best fossil record of any occasionally echinoderms. Members of the orders arthropod group, dating from at least the , and are ex- and an estimated 65,000 fossil species have been de- clusively parasitic and often have modified bodies. scribed. Most are benthic crawlers or burrowers, but Siphonostomatoids are endo- or ectoparasites of vari- many have adopted a suspension-feeding planktonic ous invertebrates as well as marine and freshwater lifesfyle, and a few are terrestrial in moist habitats. One fishes; they are often very tiny and show a reduc- species is known to be parasitic on fish gills-Sheina tion or loss of body segmentation. Poecilostomatoids orri (Myodocopida, Cypridinidae). Ostracods are parasitize invertebrates and marine fishes, and may abundant worldwide in all aquatic environments and also show a reduced number of body segments. The are known to depths of 7,000 m in the sea. Some are Platycopioida are benthic forms known primarily from commensal on echinoderms or other crustaceans. A marine cavesi the Gelyelloida are known only from few podocopans have invaded supralittoral sandy re, European groundwaters. gions (members of the family Terrestricytheridae), and members of several families inhabit terrestrial mosses Class Ostracoda and humus. Two principal taxa (ranked as subclasses Body segmentation reduced, trunk not clearly divided here) are recognized within the Ostracoda: into thorax and abdomen, with 6 to 8 pairs of limbs and . (including the male copulatory limb); trunk with 1 to 3 Myodocopans are all marine. Most are benthic, but pairs of limbs, variable in structure; caudal rami pres- the group also includes all of the marine planktonic ent; gonopores on lobe anterior to caudal rami; cara- ostracods. The largest of all ostracods, the planktonic pace bivalved, hinged dorsally and closed by a central Gigantocypris,is a member of this group. Myodocopans adductor muscle, enclosing body and head; carapace include scavengers, detritus feeders, suspension highly variable in shape and ornamentation, smooth feeders, and some predators. There are two orders: or with various pits, ridges, spines, etc.; most with one Myodocopida and Halocyprida. simple mediannaupliar eye (often called a "maxillopo- Podocopans include predominantly benthic forms; dan eye") and sometimes weakly stalked compound although some are capable of temporary swimming, eyes (in Myodocopida); adults with maxillary and (in none are fully planktonic. Their feeding methods in- some) antennal glands; males with distinct copulatory clude suspension feeding, herbivory, and detritus limbs; caudal rami (furca) present (Figure 27.20). feeding. The Podocopa are divided into three orders: Ostracods include about 30,000 described liv- the exclusively marine Platycopida, the ubiquitous ing species of small bivalved crustaceans, ranging , and the . The Palaeocopida in length from 0.1 to 2.0 mm, although some giants were diverse and widespread in the Paleozoic, but (e.g., Gigantocypris) reach 32 mm. They superficially are represented today only by the extremely rare resemble clam shrimps in having the entire body en- Punciidae (known from a few living specimens, and closed within the valves of the carapace. However, from dead valves dredged in the South Pacific). valves lack the concentric growth rings of clam shrimps, and there are major differences in the appendages. The shell is usually penetrated by pores, The Crustacean Body Plan some bearing setae, and is shed with each molt. A good deal of confusion exists about the nature of ostracod We realize that the above synopses are rather exten- limbs, and homologies with other crustacean taxa (and sive, but the diversity of crustaceans demands empha- even within the Ostracoda) are unclear-this confusion sis before we attempt to generalize about their biology. is reflected in the variety of names applied by differ- The evolutionary success of crustaceans, like that of ent authors. We have adopted terms here that allow the other arthropods, has been closely tied to modifica- easiest comparison with other taxa. tions of the jointed exoskeleton and appendages, the Ostracods possess the fewest limbs of any crusta- latter having an extensive range of modifications for a cean class. The four or five head appendages are fol- great variety of functions. lowed by 1-3 trunk appendages. Superficially, the (sec- The most basic crustacean body plan is a head ond) maxillae appear to be absen| however, the highly (cephalon) followed by a long body (trunk) with many PHYLUMARTHROPODA Crustacea: Crabs, Shrimps, and TheirKin 799

(A) Figure 21 .2O Anatomy and diversity in the class Ostracoda. (A) Anatomy ot Sclerocypris (Podocopa). Median eye (B) Anatomy of Thaumatoconcha (Myodocopa). (Continued on next page)

Sixth limb (walking leg)

Fifth limb (male) (maxilliped/clasper)

Seventh limb

(Continued on next page) 800 Chapter Twenty-One

Figure 21 .20 (continued) Anatomy and diver- sity in the class Ostracoda. (C) Internal view of (C) Antennula Metapolycope (Myodocopa), left valve removed. (D) The highly ornate Eusarsiella (Myodocopa); side view and edge view, showing the ornate shell. (E) Examples of genera from the major ostracod groups (scale bar = 1.0 mm). A: Vargula (Myodocopa, Myodocopida). B: Eusarsiella (Myodocopa, Myodocopida). C: Polycope (Myodocopa, Halocyprida). D: Cytherelloidea (Podocopa, Platycopida). Et Propontocypris (Podocopa, Podocopida). F: Macrocypris (Podocopa, Podocopida). Gi Saipanetta (Podocopa, Podocopida). H: Neonesldea (Podocopa, Podocopida). l: Triebelina (Podocopa, Podocopida). J: Candona (Podocopa, Podocopida). K: llyocypris (Podocopa, Podocopida). L'. Cyprinotus (Podocopa, Podocopida). M: Potamocypris (Podocopa, Podocopida). N: Hemicytherura (Podocopa, Podocopida). O'.Acanthocythereis (Podocopa, Podocopida). P: Celtia (Podocopa, Podocopida). Q: Limnocythere (Podocopa, Podocopida). R: Sahn i cythere (Podocopa, Podocopida). S'.Darwinula (Podocopa, Podocopida). Maxillula Fifth limb All arrows point anteriorlv. PHYLUMARTHROPODA Crustacea; Crabs, Shrimps, and TheirKin 801 similar appendages, as seen in the class Remipedia together termed the pereon. Each segment of the pe- (Figures 21.1,A.and 21,.3D,E).In the other crustacean reon is called a pereonite (= pereomere), and their ap- classes,however, various degrees of tagmosis occur/ pendages are called pereopods. The pereopods may and the cephalon is typically followed by a trunk that be specialized for walking, swimming, gas exchange, is divided into two distinct regions, a thorax and an feeding, and/or defense. Crustacean thoracic (and abdomen. All cruslaceans possess,at least primitive- pleonal) appendages might be primitively biramous, ly, a cephalic shield (head shield) or a carapace.The although the uniramous condition is seen in a variety cephalic shield results from the fusion of the dorsal of taxa. The general crustacean limb is composed of head tergites to form a solid cuticular plate, often with a protopod (= sympod), from which may arise ventrolateral folds (pleural folds) on the sides. Head medial endites (e.g., gnathobases),lateral exites (e.g., shields are found in ancient Cambrian fossil crusta- epipods), and two rami, the endopod and exopod. ceans (e.9., from the Orsten fauna), and they are char- Members of the classes Remipedia, Cephalocarida, acteristic of the classes Remipedia and Cephalocarida; Branchiopoda, and some ostracods possess append- they also occur in some former maxillopodan groups ages with uniarticulate (single-segment) protopods; and in malacostracans. The carapace is a more expan- the remaining classesusually have appendages with sive structure, composed of the head shield and a large multiarLiculate protopods (Table21.1).8 fold of the exoskeleton that probably arises (primi- The abdomen, called a pleon in malacostracans, is tively) from the maxillary somite. The carapace may composed of several segments, or pleonites (= pleo- extend over the body dorsally and laterally as well as meres), followed by a postsegmental plate or lobe, the posteriorly, and it often fuses to one or more thoracic anal somite or telson, bearing the anus (Figure 27.28). segments, thereby producing a (Figure In primitive crustaceans this anal somite bears a pair 21,.2A).Occasionally, the carapace may grow forward of appendage-like or spinelike processes convention- beyond the head as a narrow rostrum. ally called caudal rami. In the Eumalacostraca, the anal Most of the differences among the major groups of somite lacks caudal rami and is followed by a dorsal crustaceans, and the basis for much of their classifica- flattened cuticular flap; this flap is sometimes referred tion, arise from variations in the number of somites in to as the telson. the thorax and abdomery the form of their appendages, In general, distinctive abdominal appendages and the size and shape of the carapace. A brief skim- (pleopods) occur only in the malacostracans. These ming of the synopses (above) and the corresponding appendages are almost always biramous, and often figures will give you some idea of the range of varia- they are flaplike and used for swimming (e.9., Figures tion in these characteristics. 27.9-27.15). The posteriorly directed last pair(s) of ab- Uniformity within the subphylum Crustacea is dem- dominal appendages is usually different from the other onstrated particularly by the consistency of elements pleopods, and are called uropods. Together with the of the cephalon and the presence of a nauplius larva. telson, the uropods form a distinct tail fan in many Except for a few casesof secondary reductiory the head malacostracans (Figure 21,.28). of all crustaceans has 5 pairs of appendages. From an- Crustaceans produce a characteristic, and unique, terior to posterior, these are the antennules (first anten- larval stage called the nauplius (Figures 21.258,C and nae), antennae (second antennae), mandibles, maxil- 21.33D), which bears a median simple (naupliar) eye lules (first maxillae), and maxillae (second maxillae). and 3 pairs of setose, functional head appendages- The presence of 2 pairs of antennae is, among arthro- destined to become the antennules, antennae, and pods, unique to the Crustacea (as is the nauplius larva, mandibles. Behind the head segments is a growth-zone although similar "head lalae" are known from other and the telson. In many groups (e.g., Peracarida, and arthropod groups in the fossil record).7 Although the most of Decapoda), however, the free-living nauplius eyes of some crustaceans are simple, most possess a larva is absent or suppressed. In such cases,develop- pair of well developed compound eyes, either set di- ment is either fully direct or mixed, with larval hatch- rectly on the head (sessile eyes) or borne on distinct ing taking place at some postnaupliar stage (Table movable stalks (stalked eyes). 21..2).Oftenother larval stages follow the nauplius (or In many crustaceans, fro- one to three anterior other hatching stage) as the individual passes through thoracic segments (thoracomeres) are fused with a series of molts, during which segments and append- the cephalon. The appendages of these fused seg- ages are gradually added. A recent compilation of all ments are typically incorporated into the head as ad- crustacean larval forms (Martin et al. 2014) includes ditional mouthparts called maxillipeds. In the class Malacostraca, the remaining free thoracomeres are 8The term "peduncle" is a general name often applied to the basal portion of certain appendages; it is occasionally (but not always) 'Cambrian crustacean-like larvae in the fossil record termed "head used in a way that is s;rnonymous with protopod. As noted in larvae" may be precursors to the distinctive nauplius stage seen in Chapter 20, the exopod might be no more than a highly modified many modern crustaceans. See Martin et al. (2074) exite that evolved from an ancestral uniramous condition. 802 ChapterTwentv-One

TABLE 21.1 Comparison of Distinguishing Features among the 11 Crustacean Classes (and in Orders of the Class Branchiopoda and Subclasses of the Glass Eumalacostraca)

Body tagmata and Carapace or number of segments in cephalic shield each(excludingtelson) Thoracopods Maxillipeds

ClassRemipedia Cephalicshield Cephalon (6) Not phyllopodous 1 pair Trunk (up to 32)

ClassCephalocarida Cephalic shield Cephalon (6)Thorax (B) Phyllopodous None Abdomen (11)

DL.,11^-^I^..^ ClassBranchiopod4 Cephalicshield Cephalon (6) r lyruPuuuuD None OrderAnostraca Thorax (usually 11) Abdomen (usually B)

ClassBranchiopod4 Carapace Cephalon (6), Phyllopodous None Order Notostraca Thorax(11),Abdomen {mrn\/ cp()mpnfcl

ClassBranchiopod4 Carapace(bivalved, Cephalon 6,Trunk 10-32, Phyllopodous None Order Diplostraca hinged or folded) or obscured)

ClassMalacostrac4 Large,folded carapace Cephalon(6),Thorax (8), Phyllopodous None SubclassPhyllocarida coversthorax Abdomen (7)

ClassMalacostraca, Well developed Cephalon(6),Thorax (8), Not phyllopodous Five paris of thoracopods SubclassHoplocarida caraPacecovers Abdomen (6) referred to as thorax maxillipeds

ClassMalacostrac4 Carapacewell Cephalon (6),Thorax (8), Not phyllopodous; 0 to 3 pairs Subclass dorrplnnorj nr Abdomen (6) uniramous in many Eumalacostraca secondarilyreduced or lost

ClassThecostraca Carapacebivalved (at Cephalon (6),Thorax (6), Not phyllopodous, often None some stage),often Abdomen (4) reduced modified as a mantle

ClassThntulocarida Cephaiic shield Cephalon (6),Thorax (6), Not phyliopodous, None Abdomen (up to 7) qeeflrr redrrccd

ClassBranchiura Carapacebroad, Cephalon (6),Thorax (6), Not phyllopodous None eorrerino head /L,.r Abdomen (4?) \uuL 4rr^ll l-^r^r^*.\ raraLvry,/ and trunk

ClassPentastomida None Not distinguishable;body None None vermiform

ClassMystacocarida Cephalic shield Cephalon (6),Trunk (10) Not phyllopodous l pair

ClassCopepoda Cephalicshield Cephalon (6),Thorax (6), Not phyllopodous; Usually 1 pair Abdomen (5) natatory,often reduced ClassOstracoda Carapace,bivalved Subdivisionsnot clear;6-8 Not phyllopodous, None pairs of limbs reduced keys to the distinctive naupliar larvae in all groups that Swimming is usually accomplishedby a rowing ac- hatch as a nauplius as well as synopses of larval devel- tion of the limbs. Archetypical swimming is exempli- opment in all crustaceans. fied by crustaceanswith relatively undifferentiated trunks and high numbers of similar biramous append- Locomotion ages(e.g./ remipedes, anostracans/ notostracans). In Crustaceans move about primarily by use of their general,these animals swim by posterior to anterior limbs (Figure 21..21),and lateral body undulations are metachronalbeating of the trunk limbs (Figurc21.22 unknown. They crawl or swim/ or more rarely burrow, and Chapter 20). The appendagesof such crustaceans "hitchhike," or jump. Many of the ectoparasitic forms are often broad and flattened,and they usually bear (e.9.,branchiurans, certain isopods, and copepods) are fringes of setaethat increasethe effectivenessof the largely sedentary on their hosts, and most cirripedes power stroke. On the recovery stroke the limbs are are fully sessile. flexed,and the setaemay collapse,reducing resistance. PHYLUMARTHROPODA Crustacea: Crabs, Shrimps, and TheirKin 803

Compound Abdominal Antennules Antennae eyes appendages Gonopore location

Biramous I Biramous Absent A,11trunk appendages dr-protopodsof trunk segment15; similar 9 +rrrnL cemenf R

Uniramous Biramous Absent None Common poreson protopodsof lhnrarnnndc 6

Uniramous Uniramous Present None Q: on segment 1211,3or 20121,

Uniramous Vestigial Present Present (posteriorly Thoracomere11 (both sexes) reduced)

Uniramous Biramous Present A11trunk appendages Variable,on trunk segment 9 or 11, similar, or posterior or on apodous posteriorregion segmentslimbless (some Cladocera)

Biramous Uniramous Present Pleopods (posteriorly d: coxaeof thoracopods 8; reduced) Q, co*aeof thoracopods6

Tiiramous Biramous Present,well Well developed C/: coxaeof thoracopods 8; developed pleopodswith gills; Q: coxaeof thoracopods6 1 pair of uropods

Uniramous or Uniramous or Present,well Usually 5 paris of d: coxaeof thoracopods 8 or sternum biramous biramous developed nlpnnndc 1 nair of thoracomereB; nf rrrnnorlc "_ *_"r.-*" Q: coxaeof thoracopods 6 or sternum of thoracomere 6

Uniramous Biramous Absent (in None Variable;Cf openingsusually on trunk adults) selmPnt4orT:9nn14 or7

None (paired in one None Absent None Q openings on trunk segment 5 stage)

Uniramous, reduced Biramous,reduced Present None d^singleopening on thoracomere6; V gonoporesat baseof thoracopod4

None None Absent None Common gonopore,location variable

Uniramous Biramous Absent None C/ and ? openings on trunk segment 4 Uniramous Uniramous or Absent None Gonopores usually on urosomal biramous segment1 Uniramous Biramous Absent None Gonoporeson lobe anteriorto (typically) caudalrami

In members of some groups (e.9., Cephalocarida, to selectedappendages (e.9.,the pleopods of shrimps, Branchiopoda, Leptostraca), large exites or epipods stomatopods, amphipods, and isopods; the pereopods arise from the base of the le& producing broad, "leafy" of euphausids and mysids). In swimming euphau- limbs called phyllopodia. These flaplike structures aid sids and mysids the thoracopods beat in a metachro- in locomotion and may also serve as osmoregulatory nal rowing fashion, with the exopod and setal fan ex- (branchiopods) or gas exchange (cephalocardis and tended on the power stroke and flexed on the recovery leptostracans) surfaces (Figure 27.27A-C). Although sfuoke. The movements and nervous-muscular coordi- such epipods increase the surface area on the power nation of crustacean limbs are deceivingly complex. In stroke, they also are hinged so that they collapse on the comrnon mysid Gnathophausiaingens, for example, the recovery stroke, reducing resistance. Metachronal twelve separate muscles power the thoracic exopod limb movements are retained in many of the "higher" alone (three that are extrinsic to the exopod, five in the swimming crustaceans, but they tend to be restricted limb peduncle, and four in the exopodal ). 804 ChapterTwenty-One

(A)

Carpo-propodus

0)

Coxa - PHYLUMARTHROPODA Crustacea: Crabs, Shrimps, and Their Kin 805

{ Figure 21 .21 Generalized thoracic appendages of in the four primitive groups of crustaceans (cephalocarids, various crustaceans. (A-C) Biramous, phyllopodous branchiopods, phyllocarids, and remipedes) the protopod thoracopods. (A) Cephalocarida. (B) Branchiopoda. is composed of a single article. And in branchiopods and Dashed lines indicate fold or "hinge" lines. (C) Leptostraca leptostracans, the articles of the endopod are not cleady (Phyllocarida). (D) A biramous, flattened, but nonphyl- separated from one another. In the higher crustaceans lopodous thoracopod: Remipedia. (E-l) Stenopodous (Malacostraca and former "maxillopodans") the protopod thoracopods. (E) Eupfausiacea. (F) Caridea (Decapoda). comprises two or three separate articles, although in most (G) Lophogastrida (P€racarida). (H) Spelaeogriphacea former maxillopodans these may be reduced and not eas- (Peracarida). (l) lsopoda (Peracarida). Because of the pres- ily observed. In the lophogastrid (G), the large marsupial ence of large epipods on the legs of the cephalocarids, oostegite characteristic of female peracarids is shown branchiopods, and phyllocarids, some authors refer to arising from the coxa. In two groups (amphipods and them as "triramous" appendages. However, smaller epi- isopods) all traces of the exopods have disappeared, and pods also occur on many typical "biramous" legs, so this only the endopod remains as a long, powerful, uniramous distinction seems unwarranted (and confusing). Note that walking leg.

(B) Water in To head Median space (midline)

Epipods/ Exopods

Water leaves under epipods

Endite with 'filter" setae

g;5;Interlimb "filter" setae @ sPace

(E)

\y Figure 21 .22 Some aspects of locomotion (and feeding) in three crustaceans (also see Chapter 20). (A,B) Generation of swimming and feeding currents in an anostracan. (A) An anostracan swimming on its back by metachronal beating of the trunk limbs. The limbs are hinged to fold on the recovery stroke, thereby reduc- ing resistance. (B) Water is drawn from anterior to posterior along the midline and into the interlimb spaces, and food particles are trapped on the medial sides of the endites; excess water is pressed out laterally, and the trapped food is moved anteriorly to the mouth. (C-E) Locomotion in the postlarva of . (C) Normal swimming posture when moving forward slowly. (D) Sinking posture with appendages flared to reduce sinking rate. (E) A quick retreat by rapid tail flexure (the "caridoid escape reaction"), a method commonly employed by crus- taceans with well developed abdomens and tail fans. (F) A swimming remipede, Lasionectes. Note the metachronal waves of appendage movement. 806 Chaoter Twentv-One

TABLE21.2 Summary of CrustaceanReproductive Featuresa

Development type, or larval Hermaphroditic (at Parthenogenesis type at hatching least some species) Gonochoristic (in at least some species)

ClassRemipedia Nauplius (anamorphic) Yes No No

ClassCephalocarida Metanauplius (anamorphic) Yes No No -

ClassBranchiopod4 order Nauplius or metanauplius No Yes Yes /^- Anostraca \4r rau^* rurPr ^--Li^\ rrL./

ClassBranchiopod4 order Nauplius or metanauplius Yes Yes Yes Notostraca (anamorphic),or direct development

ClassBranchiopod4 order Nauplius (partly anamorphic) No Yes Yes Diplostraca

ClassOstracoda Direct, orwith bivalved nauplius/ No Yes Yes metanauplius with anamorphic development

ClassMystacocarida Metanauplius (partiy anamorphic) No Yes No

ClassCopepoda Nauplius (metamorphic) No Yes No

ClassBranchiura Metanauplius-like (partly No Yes No anamorphic), or with direct development

CIassThecostraca ? Yes Yes No

ClassTantulocarida Nauplius? + tanfulus No Yes 2 (mefamnrnhic)

ClassMalacostraca, subclass Direct development No Yes No Phyllocarida

ClassMalacostraca, subclass Zoealawa (" antizoea" or No Yes No Hoplocarida "pseudozoea")(metamorphic)

ClassMalacostrac4 Direct development No Yes No subclassEumalacostraca, superorder S1'ncarida

ClassMalacostraca, Direct development No Yes No subclassEumalacostrac4 superorderPeracarida

ClassMalacostrac4 Nauplius (metamorphic) No Yes No subclassEumalacostrac4 superorderEucarid4 order Frrnherrcienee

ClassMalacostraca, Amphion (modified zoea) (weakly No Yes No subclassEumalacostrac4 mo+emnrnhin\ superorderEucarida, order Amnhinnidacpr

ClassMalacostraca, Pre-zoeaor zoeatand with a Rare Yes No subclassEumalacostraca, nauplius in Dendrobranchiata superorderEucarida, order (metamorphic),or direct Decapoda rlorrolnnnon+

oAlso see Martin et al.201 4,Table 55.1 PHYLUM ARTHROPODA Crustacea:Crabs, Shrimps, and TheirKin 807

Recall from our discussionsin Chapters4 and 20 Comments that at the low Relmolds numbers at which small crustaceans(such as copepodsor larvae) swim Eight naupliar stages(2 orthonaupiii and 6 metanauplii), follo.rzedby about, the netlike setalappendages act not as a fil- a"pre-juvenile"stage,have been reported. tering net, but as a paddle, pushing water in front One or tvvoeggs at a time are fertilized and carried on genital of them and dragging the surrounding water along Drocessesof the firshoieonites. with them due to the thick boundary layer adher- E*bryor rrrrrulryrn"a t o- ovisacearly in developmen! resistant ing to the limb. Only in larger organisms,with (cryptobiotic) fertilized eggsaccommodate unfavorable conditions. Reynoldsnumbers approachingl,, do setoseap- Eggs briefly brooded, then deposited on substrata;resistant pendages(e.9. the feeding cirri of barnacles)begin (cryptobiotic) fertilized eggsaccommodate unfavorable conditions. to act as filters, or rakes,as the surrounding water acts lessviscous and the boundary layer thinner. Most cladoceransundergo direct development (Leptodorahatches Of course,the closertogether the setaeand setules as nauplii or metanauplii). Clam shrimps carry developing are placed, the more likely it is that their individual embryos on the thoracopodsprior to releasingthem as nauplii or motrna,rnlii boundary layers will overlap; thus densely setose appendagesare more likely to act aspaddles. Embryos usually deposited directly on substrata;many Not all swimming crustaceansmove by typical myodocopansand some podocopansbrood embryosbetween valves until hatching as a reduced adult; no metamolphosis; up to metachronalwaves of limb action. Certain plank- 8 preadult instars. tonic copepods,for example, move haltingly and depend on their long antennulesand dense se- Little studied, but apparently the eggsare laid free and up to 7 preadult stagesmay occur. tation for flotation between movements (Figure 21.18F).Watch living calanoidcopepods and you Usually with 6 naupliar stagesleading to a secondseries ot5"Iawal" stagescalled copepodites. will notice that they may move slowly by use of the antennaeand other appendages,or in short Embryos are deposlted; only Argulus is known to hatch as jerky increments/ often sinking slightly between metanauplii, others have direct development and hatch as juveniles. thesemovements. The latter type of motion results from an extremelyrapid and condensedmetachro- Six naupliar stagesfollowed by a unique iarval form ca11eda cypris nal wave of power strokes along the trunk limbs. rarva. Although the long antennaemay appearto be act- A benthic non-feeding stage,possibly a nauplius, has been reported ing as paddles, they actually collapse against the but not formally described. Development entails complex the limbs, with infective"tantulus larva." body an instant prior to the beating of thus reducing resistanceto forward motion. Some Undergo direct development in the female brood pouch, emerging other planktonic copepodscreate swimming cur- as a postlarval/prejuvenilestage called a"manca." rents by rapid vibrations of cephalic appendages/ Eggsbrooded or deposited in burrow; hatch late as clawed by which the body moves smoothly through the pseudozoealarvae, or earlier as unclawed antizoealawae. Both water. "Rowing" does occur in the swimrning crabs molt into distinct ericthus (and some into alima) larvae before settling on bottom as post-larvae or juveniles. (family Portunidae) and some deep-seaasellote isopods(e.g., family Eurycopidae),both of which A11free larval stageshave been los! eggsdeposited on substratum. use paddle-shapedposterior thoracopods to scull about. Most eumalacostracanswith well-developed Embryos brooded in marsupium of female typically formed from ventral coxal plates ca1ledoostegites; usually releasedas mancas abdomensexhibit a form of temporary, or "burst," (subjuvenileswith incompletely developed8th thoracopods). swimming that servesas an escapereaction (e.g., Brood pouch (marsupium) inThermosbaenaceaformed by dorsal mysids, syncarids,euphausids, shrimps, lobsters, caraPacecnamDer. and crayfish). By rapidly contracting the ventral Embryos shed or briefly brooded; typically undergo nauplius- abdominal (flexor) muscles,such animals shoot metanauplius-ca\ptopis -fu rcilia-juvenile developmentalseries. quickly backward, the spread tail fan providing a large propulsive surf ace (Figure 21.22C-E).This behavior is sometimescalled a tail-flip, or " cari- Eggs apparently brooded in female brood pouch; hatching likely doid escapereaction." occursas eggsfloat upward after release;hatching probably as an amphion larva (a zoea with only one pair of thoracopodsmodified Surfacecrawling by crustaceansis accomplished as mafllipeds), with perhaps 20 stagesthat metamorphose by the samegeneral sorts of leg movementsde- gradually to a subadult. scribed in the preceding chapters for insects and Dendrobranchiata shed embryos to hatch in water as nauplii or pre- other arthropods: by flexion and extension of the zoea; all others brood embryos (on pleopods),which do not hatch limbs to pull or push the animal forward. Walking until a pre-zoealor zoealstage (or later). limbs are typically composedof relatively stout, more or lesscylindrical articles (i.e.,stenopodous 808 Chaoter Twentv-One

limbs) as opposed to the broader, often phyllopodous shrimp (Diplostraca), most of which are largely en- limbs of swimmers (see Figure 27.2I for a comparison closed by their (Figures 2L.4F,G,LL,M of crustacean limb types). Walking limbs are lifted and 27.20), swim by rowing with the antennae. from the substratum and moved forward during their Mystacocarids crawl in interstitial water using vari- recovery strokes; then they are placed against the sub- ous head appendages. Most semi-terrestrial amphi- stratum, which provides purchase as they move pos- pods known as "beach hoppers" (e.g., Orchestia and teriorly through their pbwer strokes, pulling and then Orchestoidea)execute dramatic jumps by rapidly ex- pushing the animal forward. Like many other arthro- tending the urosome and its appendages (uropods), pods, crustaceans generally lack lateral flexibility at the reminiscent of the jumping of described in body joints, so turning is accomplished by reducing Chapter 22. Most caprellid amphipods (Figure 21.15E) the stride length or movement frequency on one side move about in inchworm fashion, using their subche- of the body, toward which the animal tums (like a trac- late appendages for clinging. There are also a number tor or tank slowing one tread). Many crustaceansmi- of crustacean burrowers, and even some that build grate; perhaps the most famous is the Chinese mitten their own tubes or "homes" from materials in their crab (Eriocheir sinensis),which spends most of its life in surroundings. Many benthic amphipods, for example, fresh water, but returns to the sea to breed. These crabs spin silk-lined mud burrows in which they reside. have been found over 1000 km upriver from the sea- One species, Pseudamphithoides incura arin (suborder testimony to their superb locomotory ability. Perhaps Gammaridea), constructs and lives in an unusual"bi- not unexpectedly, E. sinensisis also an important (and valved pod" cut from the thin blades of the same alga destructive) invasive species in North America and on which it feeds (Figure 21.23A). Another gammarid- Europe. It has been accidently introduced into the ean amphipod, Photis conchicola,actually uses empty Great Lakes several times, but has not yet been able to gastropod shells in a fashion similar to that of hermit establish a permanent population. crabs (Figur e 21.23C). "Hitchhiking" (phoresis) occurs Most walking crustaceans can also reverse the di- in various ectosymbiotic crustaceans, including iso- rection of leg action and move backward, and most pods that parasitize fishes or shrimps and hyperiidean brachyuran crabs can walk sideways. Brachyuran amphipods that ride on gelatinous drifting plankters. crabs are perhaps the most agile of all crustaceans. In addition to simply getting from one place to an- The extreme reduction of the abdomen in this group other in their usual day-to-day activities, many crusta- allows for very rapid movement because adjacent ceans exhibit various migratory behaviors, employing limbs can move in directions that avoid interference their locomotor skills to avoid stressful situations or with one another (and much the same thing has hap- to remain where conditions are optimal. A number of pened, independently, in many anomurans with re- planktonic crustaceans undertake daily vertical migra- duced abdomens). Brachyuran crab legs are hinged in tions, typically moving upward at night and to greater such a way that most of their motion involves lateral depths during the day. Such vertical migrators include extension (abduction) and medial flexion (adduction) various copepods, cladocerans, ostracods, and hype- rather than rotation frontward and backward. As a riid amphipods (the latter may make their migrations crab moves, its limbs move in various sequences, as in by riding on their gelatinous hosts). Such movements normal crawling, but those on the leading side exert place the animals in theirnear-surface feeding grounds their force by flexing and pulling the body toward the during the dark hours, when there is probably less limb tips, while the opposite, trailing, legs exert pro- danger of being detected by visual predators. In the pulsive force as they extend and push the body away daytime, they move to deeper, perhaps safer, water. from the tips. Still, this motion is simply a mechani- These crustaceans can form enormous shoals that cal variation on the common arthropodan walking contribute to the deep scattering layer seen on ship's behavior. Many crustaceansmove into mollusc shells sonar. Many intertidal crustaceans use their locomotor or other objects, carrying these about as added protec- abilities to change their behaviors with the tides. Crab tion. In most cases,the exoskeleton of the crustacean larvae in particular are known to migrate upward or is reduced, especially the abdomen (e.g., hermit crabs). downward according to daily rhythms, taking advan- Of course, crustaceans grow in size as they go through tage of incoming or outgoing tides to move in and out their molts, so these mobile-home-carrying crustaceans of estuaries. Some anomuran and brachyuran crabs must continually find larger shells to inhabit. Many simply move in and out with the , or seek shelter hermit crabs assemble in congregations to exchange beneath rocks when the tide is out, thus avoiding the shells in a sort of group "passing of the shells" as they problems of air exposure. One of the most interesting move into vacated larger abodes. locomotor behaviors among crustaceans is the mass In addition to these two basic locomotor methods migration of the , Panulirus nrgus, in the ("typical" walking and swimming by metachronal Gulf of and northern Caribbean. Each autumn, beating of limbs), many crustaceans move by other lobsters queue up in single file and march in long lines specialized means. Ostracods, cladocerans, and clam across the seafloor for several davs. Thev move from PHYLUMARTHROPODA Crustacea: Crabs, Shrimps, and TheirKin 809

Figure 21 .23 Amphipod "houses." (A) The complex sequence of steps in the construction of a "bivalve pod" from the brown alga Dictyota by the Caribbean amphipod Pseudamphithoides incurvaria'.('1) Initiation of cut and notch; the upper flap of the alga forms the first "valve." (2) Continuation of the cut across the algal thallus. (3) Measuring and clearing algal hairs off the second branch tip. (4) Cutting of the second valve. (5) Completed "pod" with valves attached along margins by threadlike secretions. (B) The gammaridean amphipod Grandiderella (male and female) in its silk-lined tube. The antennules and antennae are protruding from the pod entrance on the right. (C) Photis conchicola, a tem- perate eastern Pacific amphipod that spins its silken tube inside a minute snail shell, which is then carried about in the style of hermit crabs. shallow areas to the edges of deeper oceanic channels. This behavior is apparently triggered by winter storm fronts moving into the area, and it may be a means of avoiding rough water conditions in the shallows. water is drawn into an interlimb space as the adjacent appendages move away from one another, and water- Feeding borne particles are trapped by setae on the endites as With the exception of ciliary mechanisms, crustaceans the appendages then close. From here, the trapped have exploited virtually every feeding strategy imagin- particles are moved to a midventral food groove and able (and some "unimaginable"). Even without cilia, then anteriorly, toward the head. This mechanism many crustaceans generate water currents and engage of forming a boxlike "filter press" with setose phyl- in various types of suspension feeding. We have select- lopodous limbs is the typical suspension feeding strat- ed a few examples to demonstrate the range of feeding egy of cephalocarids, most branchiopods, and many mechanisms that occur in this group. malacostracans. In some crustaceans the action of the thoracic limbs Planktonic copepods were long thought to "fllter" simultaneously creates the swimming and suspension feed by generating lateral feeding gyres or currents by feeding currents. As the metachronal wave of append- movements of the antennae and mouth appendages. It age motion passes along the body, adjacent Iimb pairs was believed that these gyres swept in small particles are alternately moved apart and then pressed together, that were directly filtered by the maxillae. This clas- thus changing the size of each interlimb space (Figure sic idea of maxillary filtration, built on work by H. G. 27.22A,8; see also Chapters 4 and 20). Surrounding Cannon in the I920s, has been questioned by recent 810 Chapter Twentv-One

workers, but the model persists and is still commonly (Figure 27.24A; see also Chapter 4). Emerita are adapted presented in general works. As mentioned in Chapter to living on wave-swept sand beaches. Their compact 4, we now know that copepods and other small plank- oval shape and strong appendages facilitate burrowing tonic crustaceans live in a world of low Relmolds num- in the unstable substratum. They burrow posterior end bers, a world dominated by viscosity rather than by first in the area of shallow wave wash, with the ante- inertia. Thus, the setose mouth appendages behave rior end facing upward. Following a breaking wave, as more like paddfrs than like sieves, with a water layer the water rushes seaward, Emeritaunfurls its antennae near the limb adhering to it and formingpart of the into the moving water along the surface of the sand. "paddle." As the maxillae move apart, parcels of water The fine setose mesh traps protists and containing food are drawn into the interlimb space. from the water, and the antennae then brush the col- As the maxillae press together, the "patcel" is moved lected food onto the mouthparts. Many porcelain and forward to the endites of the maxillules, which push hermit crabs also engage in suspension feeding. By it into the mouth. Thus, food particles are not actually twirling their antennae in various patterns these ano- filtered from the water, but are captured in small par- murans create spiraling currents that bring food-laden cels of water. High-speed cinemitography indicites water toward the mouth (Figure 27.248,C). Food par- that copepods are capable of capturing individual algal ticles then become entangled on setae of the mouth ap- cells, one at a time, by this "hydraulic vacuum" meth- pendages and are brushed into the mouth by the endo- od. In fact, copepods are probably fairly selective about pods of the third maxillipeds. Many of these animals what they consume, which includes everything from also feed on detritus by simply picking up particles protistan microplankton (e.g.,diatoms) to other small with their chelipeds. crustaceans. Some mud, ghost, and lobster shrimps, such as Sessilethoracican barnacles feed by using their long, Callianassaand Upogebia(Axiidea, Gebiidea), sus- feathery, biramous thoracopods, called cirri, to fil- pension feed within their burrows. They drive water ter feed on suspended material from the surrounding through the burrow by beating the pleopods, and the water (Figure 27.16A,C,8). Studies indicate that bar- first two pairs of pereopods remove food with medi- nacles are capable of trapping food particles ranging ally directed setal brushes. The maxillipeds then comb from2 trrmto 1 mm, including detritus, bacteria, algae, the captured particles forward to the mouth. and various zooplankters. Many barnacles are also ca- Most other crustacean feeding mechanisms are less pable of preying on larger planktonic animals by coil- complicated than suspension feeding and usually in- ing a single around the prey, in tentacle fashion. volve direct manipulation of food by the mouthparts In slow-moving or very quiet water, most barnacles and sometimes the pereopods, especially chelate or feed actively by extending the last three pairs of cirri subchelate anterior legs. However, even in these cases in a fanlike manner and sweeping them rhythmically of direct manipulation, the sheer number of crusta- through the water. The setae on adjacent limbs and cean appendages adapted for feeding makes "simple" limb rami overlap to form an effective filtering net. The feeding a surprisingly complex affair, with the vari- first three pairs of cirri serve to remove trapped food ous mouthparts taking on tasks that include tasting from the posterior cirri and pass it to the mouthparts. (via sensory setae), holding, chewing, scraping, and In areas of high water movement, such as wave-swept macerating. rocky shores, barnacles often extend their cirri into the Many small crustaceans may be classified as mi- backwash of waves, allowing the moving water to sim- crophagous selective deposit feeders, employing vari- ply run through the "filter," rather than moving the ous methods of removing food from the sediments in cirri through the water. In such areas you will often which they live. Mystacocarids, many harpacticoid see clusters of barnacles in which all the individuals copepods, and some cumaceans and gammaridean are oriented similarly, taking advantage of this labor- amphipods are referred to as "sand grazerc" or "sand saving device. Iickers." By various methods these animals remove de- Most krill (euphausids) feed in a fashion similar tritus, diatoms, and other microorganisms from the sur- to barnacles, but while swimming. The thoracopods faces of sediment particles. Interstitial mystacocarids, form a "feeding basket" that expands as the legs move for example, simply brush sand grains with their setose outward, sucking food-laden water in from the front. mouthparts. On the other hand, some cumaceans pick Once inside the basket, particles are retained on the up an individual sand grain with their first pereopods setae of the legs as the water is squeezed out laterally. and pass it to the maxillipeds, which in tum rotate and Other setae comb the food particles out of the "trap" tumble the particle against the margins of the maxillules setae,while yet another set brushes them forward to and mandibles. The maxillules brush and the mandibles the mouth region. scrape/ removing organic material. Some sand-dwelling Sand crabs of the genus Emerita (Anomura) use isopods may employ a similar feedingbehavior. their long, setose antennae in a fashion similar to that Predatory crustaceans include stomatopods, remi- of bamacle cirri that "passively" strain wave backwash pedes, and most lophogastrids, as well as many species PHYLUMARTHROPODA Crustacea: Crabs, Shrimps, and TheirKin 811

Antennae

Figure 21 .24 Some crustacean feeding mechanisms feeding hermit crabs (B) Australeremus cooki and (see afso Figure 21 .22). ( ) Suspension feeding in the (C) Paguristes p/osus twirl their antennae, either in a circle sand crab Emerita. The arrows point seaward and indicate or a figure eight, to create water currents that pull food the direction of water movement as waves recede. The particles to the mouth region. (D) The predatory shrimp antennules direct water through branchial chambers. The Procaris ascensionis (Caridea) is shown here munching on antennae remove food particles from the water and then another shrimp (Typhlatya) as it holds the prey in a "cage" brush them onto the mouthparts. (B,C) The suspension formed by the pereopodal endopods.

of anostracans,cladocerans, copepods, ostracods, cir- atory behavior is particularly interesting. Its prey in- ripedes,anaspidaceans, euphausids, decapods, ta- cludes other crustaceans,particularly amphipods and naids, isopods,and amphipods. Predation typically shrimps. After Procarlslocates a potential victim (prob- involves grasping the prey with chelateor subchelate ablyby chemoreception),it moves quickly to the prey pereopods (or sometimesdirectly with the mouth ap- and graspsit within a " cage"formed by the pereopodal pendages),or even with the antennaein the caseof endopods (Figure 21,.24D).Once captured, the prey is predatory anostracans,followed by tearing, grinding, eatenwhile the shrimp swims about. Apparently the or shearingwith various mouthparts, particularly the third maxillipeds pressthe prey againstthe mandibles, mandibles.Perhaps the most highly adaptedpredatory which bite off chunks and pass them to the mouth. specialistsare the stomatopods(Figure 2L.7),which The remipedes capture prey with their rapto- possessgreatly enlarged,raptorial subchelatelimbs, rial mouth appendages(Figures 21..1.A,21.3D-F, and which they useto stabor to club and smashprey. Some 2L.22F),then immobilize the victim with an injection speciessearch out prey, but many sit in ambush at from the hypodermic maxillules.It is suspectedthat tis- their burrow entrance.The actual attack generally fol- suesare then suckedout of the preyby actionof a man- lows visual detectionof a potential prey item, which dibular mill and muscular foregut. They are probably may be another crustacean,a mollusc, or even a small alsofacultative suspension feeders and scavengers. fish. Oncecaptured and stunned or killed by the rapto- Another fascinatingadaptation for predation can rial claws, the prey is held againstthe mouthparts and be seenin many speciesof Alpheidae (the snapping shreddedinto ingestiblepieces. shrimps, e.g.,Alpheus, Synalpheus) (Figure 21.9D).In Although the cave-dwelling and often presumed such species,one of the chelipeds is much larger than "primitive" shrimp Procarisis omnivorous, its pred- the other, and the movable finger is hinged in such 812 Chapter Twentv-One

a way that it can be held open under muscle Figure 21 .25 The remarkable tension life cycle of the rhizo- > and then snapped quickly closed; this forceful clos- cephafan cirripede Peltogaster paguri, a kentrogonid ing produces a loud popping sound and a pressure parasite of hermit crabs. (A) The mature reproductive portion of the parasite (externa) produces or "shock" wave in the surrounding water. Some spe- numerous broods of male and female larvae, which are releaseo as cies appear to use this mechanism in ambushing prey nauplii (B,C) and eventually metamorphose into cypris lar- (although most alpheids are probably and vae (D). Female cyprids settle on the thorax and limbs of even include algae in their ). When feeding in a host crabs (E) and undergo a major internal metamorpho- predatory mode, the shrimp sits at its burrow entrance sis into the kentrogon form (F), which is provided with a with the antennae extended. When a potential prey pair of antennules and an injection stylet. The kentrogon,s approaches (usually a small fish, crustacean, or anne- viscera metamorphoses into an infective stage, the vermi- gon, which is transferred lid), the shrimp "pop"" its cheliped, and the resulting to the host through the hollow stylet. lnside the host, the vermigon grows with rooflets pressure wave stuns the victim, which is then quickly that ramify throughout much of the host's body; it is pulled into the burrow and consumed. These shrimps now called the interna (G). Eventually the female parasite typically live in male-female pairs within the burrow, emerges on the abdomen of the host as a virginal externa and prey captured by one individual is shared with (H). When the externa acquires a mantle pore, or aperture, its partner. Two mechanisms have been proposed it becomes attractive to male cyprids (l). Male cyprids for the production of the "pop" and associated shock settle within the aperture, transform into a trichogon form, and implant part of their wave. In some speciesthe pop seems to be created by body contents in the female,s receptacles (J). The deposit proceeds to differentiate into mechanical impact of the dactylus hammering into the spermatozoa, which fertilize the eggs of the female. propodus. A second mechanism recently proposed is (K) The dissected externa, with its rootlets, of Peltogaster, the collapse of cavitation bubbles, which are created removed from its host. Note the mantle aoedure. by the rapid closure of the claw (in excessof 100 km/ sec). Captivation occurs in liquids when bubbles form and then implode around an object (it is a well-known phenomenon damaging ship propellers). Both mecha- range from ectoparasites with mouthparts modified nisms create shock waves. Some boring (endolithic) for piercing or tearing and sucking body fluids (e.g., alpheids even use the claw snap to break off pieces of many copepods, branchiurans, tantulocarids/ several the rock into which they are digging. In some areas of isopod families, and at least one species of ostracod) to the world, populations of snapping shrimp are so large the highly modified and fully parasitic rhizocephalans, that their noise disturbs underwater communication. whose bodies ramify throughout the host tissue and In the Caribbean, colonies of alpheids have been lik- absorb nutrients directly (Figures 21.25 and2I.26). ened to those of social insects (e.g., Synalpheusregalis Rhizocephalans, which are cirripeds that have been colonies in Belize inhabit sponges and contain up to highly modified to become internal parasites of other 350 sibling males and females, and a single dominant crustaceans, are some of the most bizarre organisms in breeding female). the animal kingdom. They may have typical cirripede Many crustaceans emerge from the under nauplius and cypris larvae, but in this group the cyprid cover of darkness to feed or mate in the water column. will settle only upon another crustacean, selected to be Many predatory isopods emerge at night to feed on in- the unfortunate host. vertebrates or fish, particularly weak or diseased fish The most complex rhizocephalan life cycle is that of (or fish caught in fishing nets). the suborder Kentrogonida, which are obligate para- Macrophagous herbivorous and scavenging crusta- sites of decapods. Le this group, a settled female cypris ceans generally feed by simply hanging onto the food larva undergoes an internal reorganization that rivals source and biting off bits with the mandibles (a feeding that of caterpillar pupae in scope, developing an infec- technique similar to that of grasshoppers and other in- tive stage, called the kentrogon, beneath the cyprid exo- sects).Notostracans/ some ostracods, and many deca- skeleton. Once fully developed, the kentrogon forms pods, isopods, and amphipods are scavengers and her- a hollow cuticular structure, the stylet, which injects a bivores. Certain isopods in the family Sphaeromatidae motile, multicellular, vermiform creature called the ver- bore into the aerial roots of mangrorr" ir""r. Their ac- migon into the host. The vermigon is the active infec- tivities often result in root breakage followed by new tion stage. It has a thin cuticle and epidermis, several multiple root initiation, creating the stiltlike appear- [,pes of cells, and the anlagen of an ovary. It invades the ance characteristic of red mangroves (Rhizophora).A host's hemocoel by sending out long, branching, hollow number of crustaceans are full-time or part-time detri- rootlets that penetrate most of the host's body and draw tivores; many scavenge directly on detritus, but others nutrients directly from the hemocoel. So profound is (e.g., cephalocarids) stir up the sediments in order to the intrusion by the rootlets that the parasite takes over remove organic particles by suspension feeding. nearly complete control of the host's body, altering its Finally, several groups of crustaceans have ad- morphology, physiology, and behavior. Once the para- opted various degrees of parasitism. These animals site invades the host's gonads, parasitic castration may PHYLUMARTHROPODA Crustacea: Crabs, Shrimps, and TheirKin 813

\Er,"r.ru

Immature female Trichogon produces sperm in the receptacles

Virginal female Receptaclesempty $; +I Parasitepenetrates host abdomen I

Reproductivebody is developed from root systemwithin host o Femaledevelops into kentrogon larva and penetrateshost rl/T'|-- \ (F) (mb \4/- Kentrogon larvea *\

Kentrogon injects i;F]?:;it;.;\vermison larva into host \-u m lll /)l- < Root systemis developedwithin host Vermigon larvae (see Fig. 21.26H) 814 Chapter Twenty-One

(A)

Epidermal inclusions Cement gland (of cypris)

Carapace

Antennule glands

Thoracopods Cerebral ganglion 50 pm Cuticular reinf orcement on antennular article 1 Cernent gland canal Antennule article 2 (D)

Remnant of anterior mantle cavifz

Invasion cell Gill filament Cement gland of host of kentrogon PHYLUMARTHROPODA Crustacea: Crabs, Shrimps, and TheirKin 815

Figure 21 .26 Various stages in the life Kentrogon parasitic rhizocephalans. (See cement gland cycle of Figure 21 .25 tor a full description of a rhi- zocephalan (kentrogonid) life cycle.) (A-D) pm 20 Larvae ol Lernaeodiscus porcellanae: (A) A live cyprid. (B) A cyprid (lateral view; SEM). (C,D) Diagrams of cyprid larvae before and Cement canal after settlement (right side of carapace Antennule removed; naupliar eye omitted). The dot- 5 ted line in the second antennular article indicates the primordial kentrogon cuticle, and the placement of muscle fibers in the cyprid are indicated by arrows; the mus- Invasion cell Anterior muscles Cement canal pore cles are hypothesized to effect formation of the kentrogon and separation of the old cyprid from the kentrogon. In D, kentro- gon formation is complete. (E) A whole gill (SEM) of a host crab, Petrolisthes cabiolli' (Anomura), with several attached kentro- gons (arrows). (F) A 2-hour-old kentrogon (sagittal section). (G) A kentrogen injecting a vermigon via the stylet. (H) A vermigon. (l) A trichogon.

result (i.e.,the gonads of parasitized crabsnever pro- Members of the rhizocephalan order Akentrogonida duce mature gametes).Thus the host is transformed parasitize a much wider range of crustaceanhosts into a slave that servesthe needsof its master.The in- and do not have a kentrogon stage in their life cycle. ternal root system,or interna, eventually develops an Instead of injecting a vermigon/ the female cyprid has external reproductive body (the externa), where egg long, slender antennules that it uses to attach to the ab- production occurs.A male cyprid settleson *te extema, domen of the host, one of which actually penetratesthe transforms into a minute sexually mature instar called host's cuticle,becomes hollow, and servesfor the pas- a trichogon, and moves into the ovary-filled extema to sageof embryonic cells from cyprid larva to host. Male take up residence,where its function is to produce cyprids somehow find infected hosts and penetrate sperm. It takes only one or two trichogons to stimulate them in the samefashion as the females,releasing their the female ovaries to mature and begin releasingeggs sperm in such a way that they actually enter the body into the chamber of the externa. Externa that fail to ob- of the femaleparasite. tain male trichogons eventually die. The males are thus The akentrogonid life cycle is similar to that of the parasitic on the female (which is itself parasitic on the Kentrogonida although, in some cases,more than one crustaceanhost), and kentrogonids are gonochoris- individual parasite might infect a single host,lead- tic. A mature externa, usually arising from the host's ing to multiple externas.And in at least one'genus abdomen,will produce a successionof larval broods, (),multiple externacan develop from a sin- molting after eachlarval release(it is the only part of gle infection. The anatomy of the externa is more vari- the rhizocephalan body that molts). The larvae are leci- able than inkentrogonids, and the embryos develop di- thotrophic and develop through several nauplius stag- rectly into cypris larvae-there are no free-swimming es to the cyprid (Figures 21,.25and21.26). nauplius stages.The extreme sexual size dimorphism 816 ChapterTwenty-One

of kentrogonids does not occur in Akentrogonida, and is best developed in macrophagous decapods (scaven- no migrating trichogon stage has been observed. gers, predators, and some herbivores). Thus the food Isopods of the family Cymothoidae use modi- can be taken in quickly, in big bites, and mechanically fied mouthparts to suck the body fluids of their fish processed afterward. hosts. They attach to their host's skin or gills or, in some genera, to the tongue. One species, Cymothoa Circulation and Gas Exchange exigua, sucks so niuch blood out of its host's tongue The basic crustacean usually con- (the spotted rose snapper, in the Gulf of California) sists of a dorsal ostiate within a pericardial cav- that the tongue completely degenerates.But, remark- ity and variously developed vessels emptying into an ably, the fish doesn't die; the isopod remains attached open hemocoel (Figure 27.27). But the open hemocoel, with its clawed legs to the basal muscles of the missing which in the past led to descriptions of crustaceans as tongue, and the fish use the crustacean as a "replace- having an open circulatory system, has become highly ment tongue" to continue to feed. This is one of the modified in many groups, and in decapods at least few known cases of a parasite functionally replacing a there is a complex and intricate arrangement of true host organ it destroys. vessels that has only recently begun to be recognized. The heart is absent in most ostracods, many copepods, Digestive System and many cirripedes. In some groups the heart is re- The digestive system of crustaceans includes the usual placed or supplemented by accessory pumping struc- arthropod foregut, midgut, and hindgut. The foregut tures derived from muscular vessels. and hindgut are lined with a cuticle that is continu- The primitive heart structure in crustaceans is a long ous with the exoskeleton and molted with it (i.e., it is tube with segmental ostia, a condition retained in part ectodermally derived). The stomodeal foregut is modi- in cephalocarids and in some branchiopods, leptostra- fied in different groups, but usually includes a rela- cans, and stomatopods. Flowever, the general shape of tively short pharynx- region followed by a the heart and the number of ostia are also closely relat- stomach. The stomach often has chambers or special- ed to body form and the location of gas exchange struc- ized regions for storage, grinding, and sorting; these tures. The heart may be relatively long and tubular structures are best developed in the malacostracans and extend through much of the postcephalic region (Figure 21.27G). The midgut forms a short or long in- of the body, as it does in the remipedes, anostracans, testine-the length depending mainly on overall body and leptostracans, or it may tend toward a globular shape and size-and bears variably placed digestive or box shape and be restricted to the thorax (e.g., as in ceca. The ceca are serially arranged only in the remi- cladocerans), where it may be associated with the tho- pedes. In some malacostracans, such as crabs, the ceca racic gills (e.g., as in decapods). The intimate coevolu- fuse to form a solid glandular mass, best called a di- tion of the circulatory system with body form and gill gestive gland but sometimes called a midgut gland placement is best exemplified when comparing closely or , within which are many branched, related groups. Although isopods and amphipods, for blind tubules. The digestive gland in some crustaceans instance, are both peracarids, their are located has been shown to store lipids. The hindgut is usually largely in the pleon and in the pereon, respectively, short, and the anus is generally borne on the anal so- corresponding to the pleopodal and pereopodal gill or telson, or on the last segment of the abdomen locations. (when the anal somite or telson is reduced or lost). The number and length of blood vessels and the Examples of some crustacean digestive tracts are presence of accessory pumping organs are related to shown in Figure 21.27. After ingestion, the food ma- body size and to the extent of the heart itself. In most terial is usually handled mechanically by the foregut. non-malacostracans, for example, there are no arte- This may involve simply transporting the food to the rial vessels at all; the heart pumps blood directly into midgut or, more commonly, processing the food in the hemocoel from both ends. These animals tend to various ways prior to chemical digestion. For example, have short bodies, long hearts, or both, an arrange- the complex foregut of decapods (Figure 21.27G) is di- ment that facilitates circulation of the blood to all body vided into an anterior cardiac stomach and a posterior parts. Sessile forms, such as most cirripedes, have lost pyloric stomach. Food is stored in the enlarged por- the heart altogether, although it is replaced by a vessel tion of the cardiac stomach and then moved a bit at a pump in the thoracicans. Large malacostracans tend to time to a region containing a gastric mill, which usually have well developed vessel systems, thus ensuring that bears heavily sclerotized teeth. Special muscles associ- blood flows throughout the body and hemocoel and to ated with the stomach wall move the teeth, grinding the gas exchange structures (Figure 21.27D,8). Recent the food into smaller particles. The macerated material studies using corrosion casting techniques have shown then moves into the back part of the pyloric stomach, just how complex these vessel systems can be and have where sets of filtering setae prevent large particles from even called into question the paradigm of "open" vs. entering the midgut. This type of foregut arrangement "closed" circulatory systems in invertebrates. Large or PHYLUMARTHROPODA Crustacea:Crabs, Shrimps,and Their Kin 817

Figure 21 .27 lnternal anatomy of representative crustaceans. (A) A calanoid copepod. (B) A lepado- morph barnacle. (C) A balanomorph barnacle. (D) A stomatopod. (Continued on next page)

(B) Tergum Cirri

Scu Foregut Maxill Mandibular palp (mandible Supraesophageal Maxillary ganglion gland Adductor muscle Adductormuscle Ventral Labrum of scutum nerve mass Esophagus Rostal Supraesophageal blood ganglion sinus Depressor Maxilla Midgut muscle Digestive ceca of tergum

Stomach Testis Penis Oviduct Anus Stomach Ovary Egg mass (peduncle) Mantle in mantle cavity cavity

Sperm duct Testis Antennule Antennule

Accessory Supraesophageal (D) Anterior gland ganglion aorta Heart Optic Sperm duct Optic nerve Midgut Compound

Midgut gland Antennal artery Supraesophageal ganglion Maxillary gland

Esophagus

Subesophageal ganglion

(Continued on next page) 818 ChapterTwenty-One

(E) Anterior Cardiac Pyloric Posterior Cor frontale lateral Anterior stomach stomach artery aorta Optic artery O-stium_g""r1

Hindgut

Supraesophageal ganglion Antennal artery Ganglion Antennal nerve Venhal Antennal gland Midgut abdominal artery Midgut gland Sternal Midgut artery Subesophageal cecum Oviduct ganglion Venhal thoracic artery Anterior midgut cecum Ostia Midgut (F) Heart Anterior / Testis _ aorta )upraesopnageal ganglion Sperm duct

Antennular Penial papilla

Posterior aorta

Foregut Posterior midgut cecum Antennal gland Circumesophageal connective

Hindgut Midgut glands

(G) Lateral tooth Dorsal tooth Subesophageal of gastric mill of gastric mill ganglion

Cardiac stomach Pyloric stomach Fused ganglia Straining setae Ventral nerve cord Intestine Figure 21 .27 (continued) Internal anatomy of representative crustaceans. (E) A crayfish. (F) An amphipod. (G) The stomach of a crayfish. (H) A brachyuran crab, dorsal view with cara- pace removed. Shaining setae

active crustaceans may also possess an anterior acces- Crustacean blood contains a variety of cell types, sory pump called the cor frontale, which helps main- including phagocytic and granular amebocytes tain blood pressure/ and often a venous system for re- and special wandering explosive cells that release turningblood to the pericardial chamber. a clotting agent at sites of injury or autotomy. In PHYLUMARTHROPODA Crustacea: Crabs, Shrimps, and TheirKin 819

(H) Supraesophageal oanolinn Anterior stomach Antenna Compound eye muscle Lateral adductor muscle of mandible

Branchial chamber: Cheliped Cardiac stomach

Opthalmic artery Gilt Digestive gland

Epipod of Pereooodalmuscles first maxilliped Anterior dorsal pyloric muscle Ovary Pyloric stomach Pericardial sac Muscles of fifth pereopod Hindgut cecum Superior abdominal artery

Lateral abdominal artery non-malacostracans, oxygen is either caffied in solu- an organ with a relatively high surface area. The gills tion or attached to dissolved hemoglobin. Most mala- provide a thin, moist, permeable surface between the costracans possesshemocyanin in solution (although internal and external environments. The gills of sto- some contain hemoglobin within tissues). Hemoglobin matopods and isopods (Figure 21.28H,I) are formed uses iron as the oxygen-binding site, whereas hemo- from the abdominal pleopods. In the first case they are cyanin uses copper. The latter can give a bluish color to branched processes off the base of the pleopods, but in the hemolymph; carotenoid pigments frequently give the isopods the flattened pleopods themselves are vas- hemolymph a pale brown or orange color. Oxygen- cularized and provide the necessary surface area for binding pigments are never carried in corpuscles as exchange. Stomatopods also have epipodal gills on the they are in the vertebrates. thoracopods, but these are highly reduced. We have mentioned the form and position of gas ex- For gills to be efficient, a flow of water must be change organs (gills) for some groups of crustaceans in maintained across them. In stomatopods and aquat- the taxonomic synopses. Some small forms (e.g., cope- ic isopods a current is generated by the beating of pods, some ostracods) lack distinct gills and rely on cu- the pleopods. Similarly, the pereopodal gills of eu- taneous exchange, which is facilitated by their relative- phausids are constantly flushed by water as the ani- ly thin cuticles and high surface area-to-volume ratio. mal swims. In many crustaceans, however, the gills In the small forms of other groups a thin, membra- are concealed to various degrees and require special nous inner lining of the carapace serves this purpose mechanisms in order to produce the ventilating cur- (e.g., Cladocera, Cirripedia, Leptostraca, Cumacea, rents. In most decapods, for example, the gills are Mysida, clam shrimps, and even some members of the contained in branchial chambers formed between the Decapoda). carapace and the body wall (Figure 2L.28). Thus the Most crustaceans, however, possess distinct gills of delicate gills, while still technically outside the body, some sort (Figure 21,.28).These structures are common- appear to be (and are protected as though they were) ly derived from epipods (exites) on the thoracic legs internal organs. While such an arrangement provides that have been modified in various ways to provide a protection from damage to the fragile gill filaments, large surface area. The inner hollow chambers of these the openings to the chambers are generally small, re- gills are confluent with the hemocoel or their vessels. stricting the passive flow of water. Not surprisingly, Although their structure varies considerably (recall the the solution to this dilemma comes once again from various decapod gills described earlier), they all oper- the evolutionary plasticity of crustacean appendages. ate on the basic principles of gas exchange organs ad- Most decapods have elongate exopods on the maxil- dressed in Chapter 4 and throughout this text: the cir- lae, called gill bailers or scaphognathites, that vibrate culatory fluid is brought close to the oxygen source in to create ventilating currents through the branchial 820 ChapterTwenty-One

Blood vessels (c)

Baseof first leg

(c) Branchial (H) Attachment point to body chamber Inner carapacewall wall Epipod of first maxilliped Protopod

Body wall

Pseudotracheae

Epipod of .::.r :-.'.'::: second maxilliped

l- Merus

Sternum Coxa Basi-ischium

Figure 21 .28 Gas exchange structures. (A) Maxilla of the shrimp Pandalus. Note the setose scaphagnathite used to generate the ventilating current. (B-D) Cross sec- sand or mud with only their front ends exposed to the tions of types of decapod gills: (B) Dendrobranchiate. water. (C) Trichobranchiate. (D) Phyllobranchiate. (E,F) Paths of The positioning of the gills in branchial chambers ventilating currents through the left branchial chambers of protects them from desiccation during low tides and (E) a shrimp and (F) a brachyuran crab. (G) The branchial thus enables many chamber (cross section) of a brachyuran crab, showing crustaceans to live in littoral habi- the position of a single phyllobranchiatepodobranch. (H,l) tats; diffusion of respiratory gases commonly contin- A pfeopod of the terrestrial isopod Porcellio (sur.faceview ues even during low tides. Some decapods have even and section). Note the pseudotracheae. invaded land, especially certain crayfish and the ano- muran and brachyuran crabs known as land crabs (e.g., the hermit crab Coenobita andthe coconut crab Birgus; chambers (Figure 21.28A). These currents typically Figure 2I.IH).In these semi-terrestrial species the gills enter from the sides and rear through small openings are typically reduced in size. InBirgus the original gills around the coxae of the pereopods (called in crabs are very small, and the vascularized cuticular surface Milne-Edwards openings, after their discoverer), and of the gill chamber is used for gas exchange. Although exit anteriorly from under the carapace in the vicin- young Birgus may carry shells (or ) to protect ity of the mouth field (and antennal glands). They can their soft abdomen, adults do not and the abdomen be easily seen by observing a crab or lobster in quiet is hardened. Another striking decapod water. The flow rate of the currents can be altered, de- to life in air is displayed by the sand-bubbler crabs of pending on envirorunental factors, and can also be re- the Indo-Pacific region (family Dotillidae: Scopimera, versed, thus allowing certain decapods to burrow in Dotilla). These crabs possessmembranous discs on PHYLUMARTHROPODA Crustacea: Crabs, Shrimps, and TheirKin 821 their legs or sternites that were once thought to be au- tubule. These activities not only regulate the loss of ditory organs (tympana), but are now thought to func- metabolic wastes but are also extremely important in tion as gas exchange surfaces. water and ion balance, particularly in freshwater and The most successful crustaceans on land are not terrestrial crustaceans. the decapods, however, but the familiar sowbugs The excretion and osmoregulation carried out by an- and pillbugs. The successof these oniscidean isopods tennal and maxillary gland activity are supplemented (e.g., Porcelllo)is due in part to the presence of aerial by other mechanisms. The cuticle itself acts as a barrier gas exchange organs called pseudotrachea (Figure to exchange between the internal and extemal environ- 21.28Hj). These organs are inwardly directed, moder- ments and, as we have mentioned, is especially im- ately branched, thin-walled, blind sacs located in some portant in preventing water loss on land or excessive of the pleopodal exopods, connected to the outside via uptake of water in fresh water. Moreover, thin areas of small pores (similar to tracheae and spiracles). the cuticle, especially the gill surfaces, serve as sites of Air circulates through these sacs, and gases are ex- waste loss and ionic exchange. The epipods on the legs changed with the blood in the pleopods. Thus, in these of Branchiopoda were long assumed to function in gas animals the original aquatic pleopodal gills have been exchange (as "gills") but they are now known to serve refashioned for air breathing by moving the exchange primarily as sites of osmoregulation (hence, the taxo- surfaces inside, where they remain moist. The superfi- nomic name Branchiopoda, meaning gill-footed, is a cially similar tracheal systems of isopods, insects, and misnomer!). Phagocytic blood cells and certain regions evolved independently, by convergence, in of the midgut are also thought to accumulate wastes. association with other adaptations to life on land. In some terrestrial isopods, acfually diffuses from the body in gaseous form. Excretion and Osmoregulation Like other fundamentally aquatic invertebrates, crusta- Nervous System and Sense Organs ceans are ammonotelic, whether in fresh water or sea- The central nervous system of crustaceans is con- water or on land. They release ammonia both through structed in concert with the segmented body structure, nephridia and by way of the gills. As discussed in along the same lines as seen in other arthropods (Fig- Chapter 20, most crustaceans possess nephridial ex- ure 21.29).In the more primitive condition it is lad- cretory organs in the form of either antennal glands or derlike, the segmental ganglia being largely separate maxillary glands (Figures 21.54 and 21.27). These are and linked by transverse commissures and longitudi- serially homologous structures, constructed similarly nal connectives (Figure 21.294). The crustacean but differing in the position of their associated pores is composed of three fused ganglia, the two anterior (at the base of the second antennae or the second max- being the dorsal (supraesophageal) protocerebrum and illae, respectively). The inner blind end is a coelomic deutocerebrum, which are thought to be preoral in ori- remnant of the nephridium called the sacculus, which gin. From the protocerebrum, optic nerves innervate leads through a variably coiled duct to the pore. The the eyes. From the deutocerebrum, antennulary nerves duct may bear an enlarged bladder near the opening. run to the antennules, while smaller nerves innervate Antennal glands are sometimes called "gteerrglands." the eyestalk musculature. The third ganglion of the Most crustaceans have only one pair of these ne- brain is the posterior tritocerebrum, which presumably phridial organs/ but lophogastrids and mysids have represents the first postoral somite ganglion. The tri- both antennal and maxillary glands, and a few others tocerebrum forms a pair of circumenteric connectives (cephalocarids and a few tanaids and isopods) have that extend around the esophagus to a subesophageal well developed maxillary and rudimentary anten- or subenteric ganglion and link the brain with the ven- nal glands. Most non-malacostracans have maxillary tral nerve cord bearing the segmental body ganglia. glands, as do stomatopods, cumaceans/ and most ta- From the tritocerebrum also arise the antennary nerves naids and isopods. Adult ostracods have maxillary as well as certain sensory nerves from the anterior re- glands, but antennal glands also occur in freshwater gion of the head. species. All of the other malacostracans have antennal The nature of the ventral nerve cord often clearly glands. reflects the influence of body tagmosis. In crustaceans Blood-filled channels of the hemocoel intermingle with relatively homonomous bodies (e.g., remipedes, with branched extensions of the sacculus epithelium, cephalocarids, and anostracan and notostracan bran- creating a large surface area across which filtration oc- chiopods), the ganglia associated with each postanten- curs. The cells of the sacculus wall also actively take up nary segment remain separate along the ventral nerve and secrete material from the blood into the lumen of cord. In more heteronomous forms, however, a single the excretory organ. These processes of filtration and large subenteric ganglionic mass is formed by the fu- secretion are to some degree selective, but most of the sion of ganglia associated with the postoral cephalic regulation of urine composition is accomplished by segments (e.g., those of the mandibles, maxillules, active exchange between the blood and the excretory maxillae, and, when present, maxillipeds). The ganglia 822 ChapterTwenty-One

(A) (B) Brain Brain

Esophagus

:

Ir I (c) Thoracic Antennulary ganglia nerve I Optic nerve I Antennary I L- nerve r Esophagus Mandibular _ I nerve I Abdominal *s ganglia I \j.: Thorlcic 5, I newe plate Aj|

I

Pleon ganglia

Figure21 .29 Central nervoussystems of four crusta- brachyuran crab, wherein all thoracic ganglia have fused ceans. (A)The ladderlikesystem of an anostracan.Note and the abdominal ganglia are reduced. (D) Nervous sys- the absenceof well developedganglia in the posterior, tem of a hyperiid amphipod. Note the loss of the urosomal apodous,portion of the trunk. (B) Elongatemetameric ganglia typical of all amphipods. system of a crayfish.(C) Highlycompacted system of a

of the thorax and abdomen may also be variably fused, In decapods, hundreds of neurons can innervate each depending on segment fusion and body compaction. aesthetasc.Thermoreceptors probably occur in many For example, in most long-bodied decapods (lobsters crustaceans(those living near hydrothermal vents in and crayfish), the thoracic and abdominal ganglia are the deep seawould seemlikely candidates)but are not largely fused across the body midline, but remain sepa- yet documented. However, behaviors related to ther- rate from one another longitudinally (Figure Z1,29B). mal avoidanceand temperaturepreferences have been However, in short-bodied decapods (e.g., crabs), all shown, with thermosensitivities reported from 0.2 to of the thoracic segmental ganglia are fused to form a 2.0' C. A pair of unique sensorystructures whose func- large ventral nerve plate, and the abdominal ganglia tion is unknown, called frontal processes,occurs on are much reduced (Figure 21.29C). the head of remipedes.Many crustaceanshave dorsal Most crustaceans have a variety of sensory recep- organs,poorly understoodglandular-sensory struc- tors that transmit information to the central nervous tures on the head,which actually constituteseveral dif- system in spite of the imposition of the exoskeleton ferent types of sensorystructures that may or may not (as previously explained for arthropods in general) behomologous. (Figure 21..30).Among the most obvious of these senso- Like all arthropods,crustaceans contain well-devel- ry structures are the many innervated setae or sensilla oped proprioceptorsthat provide information about that cover various regions of the body and appendages body and appendageposition and movement during (Figure 21.3I). Studies of these structures suggest most locomotion. A few taxa within the classMalacostraca function as both mechanoreceptors (sensing touch and possessstatocysts, which either are fully closedand currents) and chemoreceptors. Most crustaceans also contain a secretedstatolith (e.g.,mysids, some an- possess special chemoreceptors in the form of clumps thurid isopods)or open to the outside through a small or rows of soft, fubular, cuticular processes called aes- pore and contain a statolith formed of sand grains thetascs (Figure 21.30,4.)located on the first antennae. (e.9.,many decapods)(Figure 21.308,C).Inthe latter PHYLUMARTHROPODA Crustacea: Crabs, Shrimps, and TheirKin 823 case the statocyst not only serves as a georeceptor, but stage is suppressed. Median eyes are in a sense"com- also detects the angular and linear acceleration of the pound" in that they are composed of more than one body relative to the surrounding water as well as the photoreceptor unit (Figure 21.30D). There are typical- movement of water past the animal (i.e., the statolith ly three such units in the median eyes of nauplii and is rheotactic). And, in some shrimp, the statocyst is ap- up to seven in the eyes of adults in which they persist. parently also engaged in hearing. Except for their basic rhabdomeric nature, however, There are two types of rhabdomeric photoreceptors the structure of median eye units is unlike that of the among crustaceans, median simple eyes and lateral ommatidia of true compound eyes. The former are in- compound eyes; both are innervated by the protoce- verse pigment cups, each with relatively few retinu- rebrum. Many species possessboth kinds of eyes, ei- lar (photoreceptor) cells. Cuticular lenses are present ther simultaneously or at different stages of develop- over the median eyes of most ostracods and some ment. The compound eyes may be sessile or stalked. copepods. Simple crustacean eyes probably function Stalked compound eyes occur in the Anostraca, many only to detect light direction and intensity. Such infor- Malacostraca, and perhaps some Cumacea (and per- mation is of particular value as a means of orientatiori haps also some trilobites). These are the only examples in planktonic forms without compound eyes, such as of moveable stalked compound eyes in the animal nauplius larvae, many copepods, etc. In some bran- kingdom. chiopods, a space above the median eye is connected The median eye generally first appears during the to the external environment by a small pore, perhaps nauplius larval stage, and for that reason it is often indicating an invagination of the eye at some point in called a naupliar eye. Like the nauplius larva itself, the distant past, although the nature and function of the median eye is thought to be an ancestral (defin- the pore is not known. ing) feature of the Crustacea; it is secondarily reduced The structure and function of compound eyes (om- or lost in many taxa in which the corresponding larval matidia) were reviewed in Chapter 20.In terms of

(c) Edge of Thread cutaway Opening to hairs cuticle statocyst rd setae

Outer row of free hairs

Large free Convex side of pigment Statolith anterolateralhairs Aesthetascs cup of ventral ocellus (chemosensorysetae) Inner rows of hair Frontal nerve supporting statolith

Suspensory band

Retinal cell

Retinal cell Connective tissue cover

Pigment cup

(at base of endopod)

Figure 21 .30 Some crustacean sense organs. (A) Aesthetascs on the antenna of the lobster Panulirus. (B) Closed statocysts in the uropodal endopods of a mysid. (C) Open statocyst in the antennules of a lobster (cutaway view). (D) A median simple eye of the copepod Telson Eucalanus (surface view). 824 ChapterTwenty-One

Figure 21 .31 Sensilla of selected crustaceans. (A) Serrate seta (mecha- noreceptor) of the second maxilliped of the anomuran $42Q. (B) Sockets of serrate setae of the third maxilliped of the cleaning shrimp Sfenopus hispidus (x228). (C) Current receptor from the anterior trunk limbs of the notostracan Triops. (D) chemosensory seta from the first pereopod of the freshwater shrimp Atya (xSZOO);note the characteristic apical pore. (E) A dual receptor (mechanoreceptor and chemoreceptor) seta from the maxilla of the remipede Spe/eonectes tulumensis (x4560). (F) Cross section of a dual receptor (micrograph and interpretive drawing;. Note the microtubules within the dendrites and the dendritic sheath that dttaches to the cuticle of the setal shaft (x17,100).

visual capacity, much more work has been done on the eyes of insects than on those of crustaceans/ and we are Dendritic sheath Microtubules left with a good deal of speculation in terms of what crustaceans actually see. Although most probably lack the visual acuity of many insects, it has been shown the ultraviolet and far-red spectra,at least to 470-570 that many crustaceans can discern shapes, patterns, nm). Stomatopods,in particular, have been shown and movement; color vision has been demonstrated to have extremely complex and sensitive eyes with a in some species (various species have been shown to wide range of capabilities. Running through the center respond to light waves from the blue-green region to of eachstomatopod eye is a midband of 6 ommatidial PHYLUMARTHROPODA Crustacea: Crabs, Shrimps, and TheirKin 825 rows-which in most species contain 4 rows that make systems is far from complete. In general, the phenom- up a color vision system with 12 visual pigments-as ena of molting (see Chapter 20), chromatophore activ- well as 2 rows that analyze both linearly and circularly ity, and various aspects of reproduction are under hor- polarized light. The ommatidia that deal with color monal and neurosecretory control. Interesting recent have a three-tier structure: the top tier contains an ul- work indicates that juvenile hormone-like compounds, traviolet-sensitive pigment, and below this are 2 tiers long thought to occur only in insects, may also occur with different pigments sensitive to wavelengths in the in at least some crustaceans. (]uvenile hormones are human visible spectrum. The upper and lower halves a family of compounds that regulate adult metamor- of each eye also have overlapping visual fields, so that phosis and gametogenesis in insects.) Bioluminescence each eye can act as a stereoscopic rangefinder. The 12 also occurs in several crustacean groups. It is common different photoreceptor types each sample a narrow set among pelagic decapods, and it has also been reported of wavelengths ranging from deep UV to far red (300 in certain myodocopan ostracods, hyperiid amphi- to 720 nm). pods, and copepod larvae. Although both insects and crustaceans have tetra- partite ommatidia, there are certain structural differ- Reproduction and Development ences between the compound eyes of insects and those Reproduction We have often mentioned the relation- of crustaceans, probably as a result of adaptation to ships between an animal's reproductive and develop- the requirements of aerial and aquatic vision. ln water, mental pattern and its lifestyle and overall survival light has a more restricted angular distributior; a lower strategy. With the exception of purely vegetative pro- intensity, and a narrower range of wavelengths than cesses such as asexual budding, the crustaceans have it does in air. Contrast is also somewhat reduced in managed to exploit virtually every life history scheme water. All of these factors place a premium on enhanc- imaginable. The sexes are usually separate, although ing the sensitivity and contrast perception of the eyes hermaphroditism is the rule in remipedes, cephaloca- of aquatic creatures. Mounting the eyes on stalks is one rids, most cirripedes, and a few decapods. Sequential dramatic way in which many crustaceans increase the hermaphroditism is not uncommon and usually is amount of information available to the eyes, by increas- expressed as protandry (individuals first mature as ing the field of view and binocular range. Eyestalks are males, then later become females), although protog- complex structural features with a dozen or so muscles yny occurs in a few species (e.g., the marine isopod controlling their movement. Gnorimosphaeromaorgonense). Irr addition, parthenogen- Typical tetrapartite compound eyes are lacking in esis is known in some branchiopods and certain ostra- the small crustaceans formerly combined as "maxillop- cods. ln one species of clam shrimp (Eulimnndia texana) odans" (copepods, barnacles, etc.), but various forms a rare type of mixed mating system exists, called and- of "compound eyes" do occur among the Branchiura, rogonochorism (i.e., androdioecy in plants), in which Ostracoda (Cypridinacea), and Cirripedia. Eyes in the males coexist with hermaphrodites, but there are no first fwo taxa most closely resemble those of other crus- true females. Androgonochorism is rare, but is also taceans in general structure and may be homologous known in the Caenorhabditiselegans, sorne with them. In the Cirripedia, the median eye and two thoracican b arnacles (e.g., Bal anus gal eatus, S calp ellum lateral eyes are all derived from a single tripartite ocel- scalpellum), and from several other branchiopod lar eye of the nauplius larva, which splits into its three crustaceans. components, each forming an adult photoreceptor fol- The reproductive systems of crustaceans are gener- lowing metamorphosis of the nauplius into a cypris ally quite simple (Figure 27.27).The gonads are derived larva. All three of these eyes thus appear to be com- from coelomic remnants and lie as paired elongate posed of simple ocelli, although the lateral eyes have structures in various regions of the trunk. In many cir- three photoreceptor cells and for this reason are often ripedes, however, the gonads lie in the cephalic region. called "compound eyes." Rhizocephalan nauplii also In some casesthe paired gonads are partially or wholly have a tripartite nauplius eye, which persist into the fused into a single mass. A pair of gonoducts extends cyprid larval stage. from the gonads to genital pores located on one of the Compound eyes are lacking altogether in many crus- trunk segments, either on a sternite, on the arthrodial tacean taxa (e.g., Copepoda, Mystacocarida, Cepha- membrane between the sternite and leg protopods, or locarida, Tantulocarida, Pentastomida, Remipedia, on the protopods themselves. Lr many crustaceans the and some Ostracoda). Members of some other groups paired penes are fused into a single median penir (".9., possess compound eyes only in late larval stages and in tantulocarids, cirripedes, and some isopods). The fe- lose them at metamorphosis (e.g., some cirripedes). male system sometimes includes seminal receptacles. Reduction or loss of eyes is also common in many deep- The position of the gonopores varies among the classes sea species,burrowers, cave dwellers, and parasites. (Table21.1). Crustaceans have complex endocrine and neurose- The curious phenomenon of intersex-having both cretory systems, although our understanding of these male and female secondary sexual characteristics-is 826 Chapter Twenty-One

Figure 21 .32 Reproduction in Crustacea. (A-D) widespread among crustaceans.Intersexual develop- Mating ) behaviors of the fiddler crab Uca. (A) Two males in ritual- ment is associated directly with the presence of endo- ized combat for the favor of a female, while she watches parasites such as bacteria and microsporidia, and it has (B). (C) A single male waving his enlarged cheliped to also been correlated with the presence of endocrine- attract a female. (D) A male fiddler crab engaged in claw- disrupting pollutants that seem to induce opposing waving behavior to attract a female. (E) A balanomorph secondary sexual characterisitcs. barnacle,with cirri and groping penis extended, impreg- Most crustaceans copulate, and many have evolved nating a neighbor. The advantage of a long penis in ses- sile animals is made obvious by this illustration.(F) courtship behaviors, the most elaborate and well Ventral views of a male and female brachyuran crab, Cancer known of which occur among the decapods. Although magister, showing the modified pleopods (setose append- many crustaceans are gregarious (e.9., certain plank- ages to retain eggs in female; modified as gonopod in tonic species, barnacles, many isopods and amphi- male). (G) A copulating pair ot Hemigrapsus sexdentafus. pods), most decapods live singly except during the (H) The planktonic copepod Sapphirina, with egg sacs. mating season. More or less permanent, or at least sea- sonal, pairing is known among many crustaceans (e.g., stenopodid shrimps; certain parasitic and commensal isopods; pinnotherid "pea" ctabs, which often live as A good deal of work has been done on fiddler crabs pairs in the mantle cavities of bivalve molluscs or in of the genus Uca (family Ocypodidae). [r these species, burrows of thalassinid shrimps). males engage in dramatic cheliped waving (of their Even the parasitic pentastomids copulate (within greatly enlarged chela, or major claw, which can ac- the host's respiratory system) and have internal fertil- count for more than 50% of the male's total mass-more ization, relying on a transfer of sperm to the female's than the largest rack of a male elk!) to atlract females and vagina by way of the male's cirri (penes). Pentastomid repel competing males (Figure 27.32A-D).In addition, early embryos metamorphose into a so-called primary males produce sounds by stridulation and substratum larva with two pairs of double-clawed legs and one or thumping, which are thought to attract potential mates. more piercing stylets (Figure 21.19F,).The larvae may Mating generally takes place once the male has enticed be autoinfective in the primary host, or they may mi- the female into his burrow. Males of some fiddler crab grate to the host's gut and pass out with the feces. In species build sand structures at the entrance of their bur- the latter case, an intermediate host is required, which row, which have been shown to athact females. may be almost any kind of vertebrate. The larvae bore Among many crustaceans/ the external sexual char- through the gut wall of the intermediate host, where acteristics are associated with the actual mating pro- they undergo further development to the infective cess. In some males, particular appendages, such as stage. Once the intermediate host is consumed by a de- the antennae of anostracans and some cladocerans, os- finitive host (usually a predator), the parasite makes its tracods, and copepods, are modified for grasping the way from the new host's stomach up the esophagus, or female. Additionall!,rrrany males bear special sperm bores through the intestinal wall, eventually settling in transfer structures, in the form of either modified ap- the respiratory system. pendages or special penes such as those of the thoraci- Mating in nonpaired crustaceans requires mecha- can barnacles (Figure 27.32E), anostracans, and ostra- nisms that facilitate location and recognition of part- cods. Examples of modified appendages include the ners. Among decapods, and perhaps many other last trunk limbs of copepods and the anterior pleopods ctustaceans, scattered individuals apparently find one of most male malacostracans (called gonopods in most another either by distance chemoreception (phero- malacostracans, or petasma in Dendrobranchiata) mones) or through synchronized migrations associated (Figure 27.32F). Sperm are transferred either loose in with lunar periodicity, tidal movements, or some other seminal fluid or (in many malacostracans and in cope- environmental cue. Contact pheromones are also pods) packaged in spermatophores. Motile flagellated utilized. Males of some marine myodocopan ostracods sperm occur only in some of the former maxillopodan (some Halocyprididae, some Cypridinidae) produce groupsi in other crustaceans the sperm are nonmotile. complex bioluminescent displays, similar to those of Crustacean sperm are highly variable in shape, even fireflies, to attract females. Once prospective mates are bizate in many instances, often being large round or near each other, recognition of conspecifics of the op- stellate cells that move by pseudopods or are, seem- posite sex may involve several mechanisms. Over 60 ingly, nonmotile.e Sperm are deposited directly into speceis of cypridinid ostracods engage in luminescent the oviduct or into a seminal receptacle in or near the courtship behavior in the Caribbean alone. Apparently, female reproductive system. In some crustaceans most decapods employ chemotactic cues requiring actual contact. Vision is known to be important in the eThe stenopodid shrimps (most of which live in pairs), in sperm of freshwater ostracods are the longest in the animal kingdom, relative to body (up certain anomurans (e.9., size to 10x body"length). Even the family Porcellanidae), and though their sperm are aflagellate, they are filiform and range inbrachyurans (many grapsids and ocypodids). from several hundred microns to millimeters in leneth. PHYLUMARTHROPODA Crustacea:Crabs, Shrimps,and Their Kin 827 828 ChapterTwenty-One

'La ,/A\ 'La 1b (B) Dorsal

Mandibular Antennal ectoderm ectoderm Antennular Postnaupliar ectoderm ectoderm I I 2d Protocerebral I I ectoderm i I 3c aa Midgut I I (entoderm) 2b

(G)

First

Telson

Figure 21 .33 Cleavage and posthatching stages among crustaceans. (A) Modified holoblastic spiral cleavage has produced a 28-cell embryo of the cirripede Tetraclita. The cells are labeled as in Wilson's coding system. (B) A fate map of a cirripede blastula (right-side view). (C) Intralecithal nuclear divi- sions in the early cleavage of a mysid. (D) Newly hatched copepod nauplius larva. (E) Nauplius of a copepod. (F) Settling and metamorphosis of a cypris larva of a lepadomorph barnacle. (G) The zoea ("mysis") stage larva of the dendrobranchiate shrimp Penaeus. (H) Zoea larva of the brachyuran crab . (l) Zoea larva of a porcelain crab. (J) Megalopa larvae of the xanthid crab . (K) The characteristic antizoea larva of a sto- matopod. (L) The translucent, paper-thin phyllosoma larva of the lobster Jassa. (M) Cryptoniscus stage (not a true larva) of the epicaridean isopod probopyrus bithynis. (N) Cyprid larva of a barnacle.

femalescan storesperm for long periods(e.g., several embryos in a marsupium, a ventral brood pouch yearsin the lobsterHomarus), thus facilitating multiple formed from inwardly directed plates of the leg coxae broods from single inseminations. called oostegites (thermosbaenaceans are an excep- The great majority of crustaceansbrood their eggs tion among the Peracarida and use the carapace as a until hatching occurs,and a variety of brooding strat- brood chamber). Other crustaceans attach the embryos egieshas evolved. Peracaridsbrood the developing to endites on the bases of the legs or to the pleopods PHYLUMARTHROPODA Crustacea: Crabs, Shrimps, and TheirKin 829

Antennule

Antenna First thoracopod

Secondthoracopod

Pleotelson

little about their embryology. The eggs are centro- lecithal, with various amounts of yolk. The amount of yolk greatly influences the type of early cleavage and is often related to the time of hatching (Chapter 4). As (Figure 21..32F),usually using mucus secreted by spe- far as is known, the zygotes of most non-malacostra- cialized glands. In some cladocerans, brooding takes cans undergo some form of holoblastic cleavage, as do place in a dorsal brood chamber formed by the cara- those of slmcarids, euphausids, penaeids, amphipods, pace. However, the slmcarids, almost all dendrobran- and parasitic isopods. However, cleavage patterns are chiate shrimps, and most euphausids shed the zygotes extremely variable, ranging from equal to unequal directly into the water. A few others deposit their fertil- and from radial-like to spiral-like. The occurrence of ized eggs in the environment, usually attaching them modified spiral cleavage (Figure 21.33A) reported from to some object (e.g.,branchiurans, some ostracods, some crustaceans had generally viewed as evidence many stomatopods). These deposited embryos may be of close ties between the crustaceans and other spira- abandoned or, as is the case in stomatopods, carefully lian groups such as the . However, the gen- tended by the female. Nonetheless, parental protection erality of spiral-like cleavage among crustaceans has of the embryos until they hatch as larvae or juveniles been called into question with evidence from molecu- is typical in crustaceans. Thus, crustaceans usually en- lar phylogenetics that indicates arthropods belong to gage in mixed or direct life histories (Table21..2). the clade of Protostomia, not the Spriralia (where annelids are nested). And in some crustacean Development Although crustaceansare the most groups, the cell lineages and germ layer origins are widespread animals on Earth, we know surprisingly quite different from those of typical spirally cleaving 830 ChaoterTwentv-One embryos. For example, in barnacles the mesodermal subsequent phases, with each phase containing slightly germ layer arises from the 3A, 3B, and 3C cells, and different morphological steps called stages, before the the 4d cell contributes to ectoderm (Figure 21'338)- adult condition is achieved. Direct development oc- whereas typical spiral cleavage involves a 4d origin of curs in some cladocerans and branchiurans, and in mesoderm. Euphausids were long thought to have spi- all ostracods, phyllocarids, slmcarids, and peracarids. ral cleavage, but recent work indicates they do not- Ostracods are tlpically viewed as having direct devel- only the oblique ahgle of the mitotic spindles during opment, and they lack a distinct larval stage. However, the transition from the 2- to the 4-cell stage resembles some ostracod species hatch with only the first three spiral cleavage. There are also differences between pairs of appendages present, and they are thus true various crustacean and other arthropod taxa involving nauplii, even though they are in a bivalved carapace the positions of the presumptive germ layers relative to and add limbs gradually (the juvenile instars resemble one another, especially the endoderm and mesoderm. miniature adults). All other crustaceans have some We want to emphasize, however, that such variations form of mixed development. The larval stages that are not surprising in such a diverse and ancient taxon have been recognized in crustacean groups that under- and do not negate the fundamental similarities that go mixed development have been assigned a plethora unite the Arthropoda. of names, and the homologies among these forms are Meroblastic cleavage is the rule among many mala- not always understood. The more commonly encoun- costracans.Here again, the exact pattern varies, but it tered developmental forms are summarized below generally involves intralecithal nuclear divisions fol- (also see Table 21.2 and Figure 21..33),but we do not lowed by nuclear migration to the periphery of the em- attempt to describe them all bryo and subsequent partitioning of the nuclei into a Crustacean development is sometimes described as cell layer around a central yolky mass (Figure 21'.33C). being either epimorphic, metamorphic, or anamorphic. The form of the blastula and the method of gastrula- Flowever, we caution readers that a clear evolution- tion are dependent primarily on the preceding cleav- ary and functional understanding of crustacean de- age pattern and hence ultimately on the amount of velopmental stages is still lacking, and thus the terms yolk. Holoblastic cleavage may lead to a coeloblastula "rrtixed" and "direct" may be preferable, and less am- that undergoes invagination (as in syncarids) or in- biguous, until we have a better understanding of this gression (as in many copepods and some cladocerans phenomenon. and anostracans). Other crustaceans form a stereoblas- Epimorphic development is direct; in crustaceans it tula followed by epibolic gastrulation (e.g., cirripedes). is thought to result from a delay in the hatching of the Most cases of meroblastic cleavage result in a periblas- embryo, which causes the nauplius (and any other pos- tula and the subsequent formation of germinal centers. sible larval stages) to be suppressed or absent. Crustaceans share a characteristic larval stage known Metamorphic development is the type of extreme as the nauplius larva, denoted by the appearance of three mixed development seen among the Eucarida; it in- pairs of appendage-bearing somites (Figure 21.33D).10 cludes dramatic transitions in body form from one life In those groups having little yolk in their eggs, the nau- history stage to another. (This pattem is similar to holo- plius is generally free living. In those species with yolky metabolous development in insects-for example, the eggs, the nauplius stage is generally passed through as transformation of a caterpillar into a butterfly.) In gen- part of a longer period of embryonic development (or eral, up to five distinct preadult, or larval, phases may a long brood period), and it is sometimes referred to as be recognized among crustaceans: nauplius, meta- an egg nauplius. Free-living nauplii are usually plank- nauplius, protozoea, zoea, and "postlarva." The zoeal totrophic, and their release corresponds to the depletion phase shows the greatest diversity in form among the of stored yolk. However, in a few groups of crustaceans various taxa, and especially in decapods it has been (e.g., euphausids and dendrobranchiate shrimps), the given different names in different grouPs (e.g., acan- nauplius exhibits lecithotrophy. thosoma, antizoea, mysis, phyllosoma, pseudozoea). It Crustacean development is either direct, with the is common for the zoeal phase to contain a large num- embryos hatching as juveniles that resemble miniature ber of stages, each differing only slightly from the one adults, or mixed, with embryos brooded for a brief or preceding it.1l Regardless of name, zoea ate character- prolonged period and then hatching as a distinct lar- ized by the presence of natatory exopods on some or all val form. These larval forms may pass through several of the thoracic appendages and by the pleopods being absent (or rudimentary). Use of the term "postlarva"

10It is unfortunate, as these stages differ dramatically from was not until J. V. Thompson discovered the nauplius lawae of barnacles in the nineteenth century that this group was finally the preceding larvae as well as from the adults; they classified as Crustacea, a discovery that also marked the first use of iarval features in understanding the phyiogeny of marine invertebrates. A recent atlas of crustacean larvae (Martin et al. 11Thezoea larvae of panulirid lobsters (phyllosoma larvae) are 2014) includes historical notes on larval development in all major lar ge, bizart e-appearing creatures (Figure 21.33L), which can crustacean groups. occur in such large numbers as to be a favorite food of . PHYLUMARTHROPODA Crustacea: Crabs, Shrimps, and TheirKin 831 represent unique transitional stages (both morphologi- From this wealth of terms and diversity of develop- cally and ecologically). Examples in the Decapoda in- mental sequences/ we can draw two important gener- clude the megalopa of true crabs and the puerulus lar- alizations concerning the biology and evolution of the vae of spiny lobsters. In this phase of development, the crustaceans. First, different developmental strategies role of swimming has switched from the thoracopodal reflect adaptations to different lifestyles. In spite of limbs to the appendages of the abdomen. many exceptions, we can cite the early release of disper- Anamorphic development is a less extreme type of sal larvae by groups with limited adult mobility, such indirect development in which the embryo hatches as a as thoracican barnacles, and by those whose resources nauplius larva, but the adult form is achieved through may not permit production of huge quantities of yolk, a series of gradual changes in body morphology as such as the copepods. At the other end of this adaptive new segments and appendages are added (it is similar spectrum is the direct development of peracarids-a in many ways to hemimetabolous development in in- major factor allowing the invasion of land by certain sects).In other words, the postnaupliar stages gradu- isopod lineages. Between these extremes we see all de- ally take on the adult form with succeeding molts; the grees of mixed life histories, with larvae being released classic example of anamorphic development is often at various stages following brooding and care. Second, said to be the Anostraca. Cephalocarida, Remipedia, because developmental stages also evolve, an analysis many Branchiopoda, and Mystacocarida are anamor- of developmental sequences can sometimes provide phic-the nauplius larva grows by a series of molts information about the radiation of the principal crusta- that add new segments and appendages gradually as cean lineages. For example, the evolution of oostegites the adult morphology appears. In many groups hatch- and of direct development combine as a unique syn- ing is somewhat delayed, and the emergent nauplius apomorphy of the Peracarida. Similarly, the addition larva is termed a metanauplius. The basic nauplius pos- of a unique larval form, such as the cypris larva that sessesonly three body somites, while the metanauplius follows the nauplius in the cirripedes, can be viewed has a few more; however, both possessonly three pairs as a unique specialization that demarcates that group of similar-appearing appendages (which become the (Cirripedia). The cyprid either hatches as the only free- adult antennules, antennae, and mandibles). The end of living larva, or it is the final larval stage after a series of the naupliar/metanaupliar stage is defined by the ap- lecithotrophic or planktotrophic nauplius larval stages. pearance of the foffth pair of functional limbs, the max- It should also be noted that the branchiopods and illules. In copepods a postnaupliar stage called a copep- some freshwater ostracods have evolved specialized odite (simply a small juvenile) is often recognized. ways of coping with the harsh conditions of many fresh- The most extreme forms of metamorphic, or mixed, water environments. Parthenogenesis, for example, is development occur in the malacostracan superorder conunon in freshwater ostracods. Other adaptations in- Eucarida. The most complex developmental sequences clude production of special overwintering forms, usu- are seen among the dendrobranchiate shrimps, which ally eggs or zygotes that can survive extreme cold, lack hatch as a typical nauplius larva that eventually under- of water, or anoxic conditions. Perhaps most remark- goes a metamorphic molt to become a protozoea larva, able in this respect are the large-bodied branchiopods with sessile compound eyes and a full complement of (fairy shrimp, tadpole shrimp, and clam shrimp) whose head appendages. The protozoea, after several molts, encysted embryos are capable of an extreme state of an- becomes azoea larva, with stalked eyes and three pairs aerobic quiescence, or diapause. During these resistant of thoracopods (as maxillipeds). The zoea eventually stages, the metabolic rate of the embryos may drop to yields a juvenile stage (the "postlawa," a better term less than 10% of their normal rate. for which is "decapodid") that resembles a miniature Many crustaceans have indeterminate growth, adult, but is not sexually mature. In some other eucarid that is, they continue to molt throughout their life. In groups (Caridea and Brachyura) the postlarva is called contrast, other species have determinate growth and a megalopa, and in the Anomura it is often called a ceasemolting following puberty (this life history stage glaucothoe; in both casesthere are setosenatatory is sometimes referred to as the terminal molt, or ter- pleopods on some or all of the abdominal somites. In minal anecdysis). In some species, the terminal molt other eucarids, some (or all) of these stages are absent. is sex specific; for example, in American blue crabs Various other terms have been coined for different (Callinectessapidus) only females have a terminal molt. (or similar) developmental stages. For example, the modified zoeal stagesof some stomatopods are called antizoea and pseudozoea larvae, and the advanced Crustacean Phylogeny zoeal stage of many other malacostracans is often called a mysis larva. In euphausids, the nauplius is fol- Countless phylogenetic studies have been published lowed by two stages, the calyptopis and the furcilia, on the topic of crustacean evolution. General agree- which roughly correspond to protozoea and zoea stag- ment has been reached in some areas, but despite a es, before the juvenile morphology is attained. great deal of effort, many fundamental mysteries re- 832 Chapter Twentv-One main unsolved, including the broad structure of the Thecostraca (barnacles and their kin), and Mala- Pancrustaca tree. The use of molecular gene sequence costraca, but challenged others, and proposed sev- data in crustacean phylogenetics is only just beginning. eral new names and clades (e.g., Oligostraca and \ /hile in some casesit has resolved longstanding issues Vericrustacea) that have yet to withstand the test of or confirmed previous hypotheses, in other casesit has time. led to still more qlrestions. There are several particu- In the 1950s,Russian biologist W. N. Beklemischev larly problematic i3sues. What are the basalmost living and Swedish carcinologist E. Dahl independently pro- crustaceans, what sort of body did they have, and what posed that the copepods and several related classes are the relationships among them? What are the rela- constitute a monophyletic clade. Dahl proposed the tionships of, and among, the taxa that were once united class Maxillopoda for these taxa, and that term has as "maxillopodans" (the copepods, branchiurans, the- been employed often since then. Characters shared by costracans, tantulocarids, mystacocarids, and pentas- these small taxa include the shortening of the thorax to tomids)? Where do the Ostracoda, Cephalocarida, and six or fewer segments and of the abdomen to four or Remipedia fit into crustacean phylogeny? \A/hat are the fewer segments, reduction of the carapace (or, in the relationships among the Peracarida, especially of the case of ostracods and cirripedes, extreme modifica- many orders and families of Isopoda and Amphipoda? tion of the carapace), loss of abdominal appendages, What are the major decapod lineages and how are they and other associated changes, all thought to be tied to related to one another? What group of crustaceans is early paedomorphic events during the larval (or post- represented by the mysterious "y-larvae" (the Faceto- larval) stage of this lineage as it began to radiate (an tecta), beyond the subsequent sluglike ypsigon stage idea first proposed in\942 by R. Gurney). However, that is clearly still not an adult? And, of course, what is molecular phylogenetic studies since then have shown the crustacean to the Hexapoda? Maxillopda to be a nonmonophyletic grouping, and Debates on crustacean phylogeny often center on the taxon has been abandoned by most modern work- whether paddle{egged Crustacea are ancestral or de- ers. Yet two of those groups, the copepods and thecos- rived. The paddle-legged ancestry hypothesis holds tracans, have since been reunited in one study (Oakley that the first crustaceans had leaflike (phyllopodous) et al. 2013) that posits a clade (the ) based thoracic legs that were used both for swimming and on the same number (6) of naupliar larval stages in for suspension feeding, as seen in the living cephalo- these groups. carids, leptostracans, and many branchiopods. Or that The monophyletic nature of the class Malacostraca the first crustaceans had simple, paddle-like legs that has rarely been questioned. Within the Malacostraca were used for swimming, but not for feeding; instead, are two clades: Leptostraca, which have phyllopo- the tasks of feeding were undertaken by the cephalic dous limbs and seven abdominal somites, and appendages-a plan perhaps best represented among Eumalacostraca, which lack phyllopodous limbs living crustaceans by the remipedes. However, the op- and have six abdominal segments. Whether the posing view, that paddle-legged crustaceans are more Hoplocarida are members of the Eumalacostraca or derived, is supported by the recent multigene studies. deserving of their own subclass of the Malacostraca is A large molecular study suggested a highly-derived still a subject of debate, but we consider them a sepa- sister group relationship between the two most many- rate subclass here. Hoolocarids and eumalacostracans segmented and "wormlike" groups, the cephalocarids also have the sixth abdbminal appendages modified as and remipedes, both being paddle-legged groups, unit- uropods (which work in conjunction with the telson as ing them in a proposed clade (called Xenocarida) that a tail fan). Relationships among the three main eumala- would be the sister to the hexapods (Regier et aI.2010; costracan lines (syncarids, peracarids, and eucarids), Figure 21,.348).Another recent phylogenomic study and even within the Eucarida, are far from settled and concluded that Remipedia are the closest extant rela- have provided zoologists with many generations of tives of insects (Misof ela!.201.4),and some compara- lively debate. tive neurological work also supports this view. In con- The class Branchiopoda is usually monophyletic in trast, a traditional, morphology-based phylogeny of molecular analyses, but it is difficult to define on the the Crustacea hypothesizes a paddleJegged ancestry, basis of unique synapomorphies because it shows such but places the Remipedia at the base of the crustacean great morphological variation. But larval (naupliar) tree (Figure 2I.34A). Comparative spermatological characters, such as the reduced and tubular first anten- studies, on the other hand, seem to ally the remipedes na and uniramous mandibles, strongly support their with certain former maxillipodans. Clearly, we have a monophyly, as do almost all studies employing molec- good way to go before we will deeply understand the ular data. As is true with so many crustacean groups, phylogeny of Crustacea. our early classifications greatly underappreciated their The Regier et al. (2010) study, summarized here diversity, and relationships among the constituent in Figure 27.348, strongly supported some tradition- groups are far more complex than was first thought. ally recognized groupings, such as Branchiopoda, Apparently some branchiopods have secondarily lost PHYLUMARTHROPODA Crustacea: Crabs, Shrimps, and TheirKin 833

.|9 (A) t\' |p f)- 'b' .nY :c- .nlY .ti' .o ^t\ rq\ ^*oS -.{o"-a{o" v' ,o? .o, | .Ae";9" | {\- {C' | '

Ostracoda 11 10 Branchiura, Pentastomida, Mystacocarida 9

8 Branchiopoda 7

6 Copepoda

Thecostraca (barnacles and their kin)

Malacostraca

.'\ Figure 21 .34 Two competing views of evolution within Lepnalocarrdal-l the Crustacea. (A) A traditional view of crustacean rela- Xenocarida tionships, with paddle-legged Crustacea at the base. The I Remipedia ) morphological synapomorphies depicted on the clado- gram are as follows (1-5 represent synapomorphies of the subphylum "Crustacea"): 1: head composed of 4 or 5 fused segments (plus acron) with 2 pairs of antennae and 2 or 3 pairs of mouth appendages; 2: biramous second antennae; 3: nauplius lawa; 4: phyllopodous body limbs with maxillopodan naupliar eye; 23'. thorax of 6 or fewer (with large epipods); 5: with head shield or small cara- segments; 24: abdomen of 4 or fewer segments; 25: pace; 6: raptorial mouth appendages; 7: mouth append- genital appendages on the first abdominal somite (associ- ages situated in posteriorly directed atrium; 8: anterior ated with male gonopores); 26: B-segmented thorax and thoracopods (one or more pairs) modified as maxillipeds 7-segmented abdomen (plus telson); 27: male gonopores (a highly variable trait that occurs in remipedes, malacos- fixed on thoracomere 8/females on thoracomere 6; 28: tracans, and some former "maxillopodans"); 9: loss of carapace forms large "folded" structure enclosing most of phyllopodous condition on trunk appendages; '10: trunk body; 29: abdomen reduced to 6 segments (plus telson); appendages oriented laterally;11: maxillulesfunction as 30: last abdominal appendages modified as uropods and .1 hypodermic fangs; 2: postcephalic trunk regionalized as forming tail fan with telson; 31: caridoid tail flip locomo- thorax and abdomen; 13: loss of internalorgan homon- tion (escape reaction); 32: thoracopods with stenopodous omy (e.9.,segmental gut ceca); '14:reduction in number endopods; 33: replacement of thoracic suspension feed- of body segments; 15: reduction of abdomen (to 11 seg- ing and phyllopodous thoracic limbs with cephalic feeding ments); 16: fully developed carapace (reduced in several and nonphyllopodousthoracic limbs. Note that loss of subsequent lineages); 17: reduction of abdomen to fewer the phyllopodous trunk limbs (character 9) has occurred than 9 segments; 18: reduction (or loss) of abdominal several times, in the Remipedia, Eumalacostraca, some appendages; 19: first and second maxillae reduced or Iineages of Branchiopoda, and most of the former "maxil- lost; 20: thorax shortened to fewer than 11 segments; lopodan" groups. (B) Phylogeny of the clade 21: abdomen shodened to fewer than 8 seomentsi 22i as derived by Regier et al. 20'10. the carapace, and others have secondarily lost most or realizationrenders the group called Crustaceapara- all of the abdominal appendages. phyletic. The monophyletic clade containing both That a group of crustaceans gave rise to the mega- crustaceansand insectsis most often referred to as the diverse group of arthropods called the Hexapoda (in- Pancrustacea(see Chapter 20),but it is also sometimes sects and their kin) is now almost universally agreed called the Tetracorrata,a name that recognizesthe upon, based on a wide array of evidence that includes squareshape of the ommatidia of many species.Earlier molecular sequence data and neuroanatomy. This work suggestedthat Branchiopodawas the likely sister 834 Chapter Twenty-One

group to Hexapoda, but recent researchsupports the opportunity for evolutionary experimentation.Any origin of the Hexapoda from either the Remipedia conceivablecladogram of crustaceanphylogeny will or a remipede-cephalocaridclade-the later group- require the acceptanceof considerablehomoplasy. ing (Remipedia-Cephalocarida-Hexapoda)has been Fossil data (including that of the Orsten fauna, named Miracrustacea,meaning "surprising crusta- Figure 2L.35)seems to favor phyllopodous limbs asthe ceans."Like the arthropods in general,crustaceans primitive condition. However, developmental studies exhibit high levels of evolutionary parallelism and following the expressionof Distal-Iessandother devel- convergenceand many apparentreversals of character opmental genessuggest that the early embryogeny of states.This genetic flexibility is no doubt due in part to limbs is very similar among crustaceans.For example, the nature of the segmentedbody, the serially homolo- trunk limbs always emerge as ventral, subdivided gous appendages,and the flexibility of developmental limb buds. In phyllopodous limbs, the subdivisions genes/which, as we have stressed,provide enormous of theselimb buds grow to becomethe endites and PHYLUMARTHROPODA Crustacea: Crabs, Shrimps, and TheirKin 835

Figure 21 .35 (A-E) Examples of Upper Cambrian (-510 Ma), prob- ably meiofaunal crustacean fossils from the spectacular Swedish Orsten deposits. This ancient crustacean fauna possessed the key attributes of modern Crustacea, including compound eyes, head shields/carapaces, naupliar larvae (with locomotory first antennae), and biramous appendages on the second and third head seg- ments (the second antennae and mandibles). (A) Bredocaris. (B) Rehbachiella, an early branchiopod, lateral (drawing) and ventral (SEM) views. (C) Skara, drawing and SEM. (D) Cambropachycope clarksoni, a bizarre species with an expanded head and two pairs of enlarged thoracopods, drawing and SEM. (E) Maftinssonia elongata, SEMs of first larva and postlarval stage. (F) Ercaia minuscula, an early Cambrian (520 Ma) crustacean from South .

larvae are only a couple hundred microns long; adults are about 1 mm in length). Sknra and many other Orsten Crustacea were probably meiofaunal animals not un- like modern marine meiofaunal crustaceans (e.g., the mystacocarids). Dozens of Orsten microcrustacea have so far been described (Figure 21.35).Recently, a beauti- fully preserved fossil crustacean, Ercain minuscl;Ia, was described from the middle Cambrian (520 Ma) of South China. It has an untagmatized, L3-segmented trunk with serially repeated biramous appendages and a head with stalked eyes and five pairs of head append- the endopod of the natatory / filtratory adult limbs. In ages, including two pairs of antennae. Ercaia minuscu- stenopodouslimbs, the samelimb bud subdivisions la is only 24rrrm long (hence the species name), and end up developing into the actual segmentsof the bears resemblances to both cephalocarids and maxil- adult limb. Hence, the endites of phyllopodous limbs lopodans (Figure 21.35F). appear to be homologous to the segmentsof the steno- Studies on the Swedish Orsten fauna (510 Ma), the podous limbs. This discovery supports an emerging Middle Cambrian (520 Ma) Burgess Shale-like deposits view of developmental plasticity in arthropod limbs, from around the world, and the Lower Cambrian (530 and it suggeststhat relatively simple genetic "switch- Ma) Chengjiang fossils from China have shown that es" can account for major differencesin adult mor- Cambrian Crustacea had all the attributes of modern phologies. Thus, it is quite plausible that stenopodous crustaceans, such as compound eyes/ an acron, distinct limbs have evolved multiple times from phyllopodous head and trunk tagmata, at least four head append- ancestors,and this is the scenariodepicted in the clado- ages, a carapace (or head shield), naupliar (or "head") gram in Figure 21.344. larvae (with locomotory first antennae), and biramous Work by Klaus Miiller and Dieter Waloszekon appendages on the second and third head somites three-dimensionallypreserved microscopic arthropods (the second antennae and mandibles). We now,know from the middle Cambrian Orsten (around 510Ma) de- that the crustaceans are an ancient group. Their fossil posits of Swedenhas documenteda diversefauna of record dates back to the early Cambrian, or likely the minute crustaceansand their larvae.Among them, for Ediacaran period if some arthropod fossils from ihose example, is Skara(Figure 21..35C),a cephalocarid- or strata are viewed as Crustacea. The earliest known mystacocarid-like crustaceanfor which both naupliar crustacean larval stage is a fossil of a slightly ad- larvae and adults have beenrecovered (the nauplius vanced nauplius (called a metanauplius) from the early 836 Chapter Twenty-One

Cambrian (525 Ma) of China that in many ways re- within the Crustacea, such as the cirripedes, that were sembles the naupliar larvae of modern cirripedes. This already becoming distinct. Depending on one's defini- is remarkable, as it confirms not only of the great age tion of "CrtJslacea," it may even be that the first arthro- of the Crustacea as a whole but also the age of groups pods were themselves crustaceans.

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