CRUSTACEA 255

CRUSTACEA species that can be classified as stygobites. Subterranean םThe taxonomic status of crustaceans has long been debated by 20 carcinologists (the scientists who study these arthropods). The cladocerans (particularly hyporheic species) are known from all group has been assigned to one of the phylum, subphylum, continents and most demonstrate only minor troglomorphic ad- or superclass levels, with five, six, and even ten classes being aptations. recognized. The purpose of this essay is not to enter into a taxonomic debate, but to recognize that crustaceans are one of Class Remipedia the oldest arthropod groups and certainly represent one of the Remipedia (Figure 1a) are among the most primitive of all extant largest, most diverse, and most successful groups of invertebrates crustaceans. Twelve species, placed in two families containing six on Earth, with some 40 000 species recognized (Hobbs, 2000). genera (Cryptocorynetes, Godzilliognomus, Godzillius, Lasionectes, Although crustaceans occupy a truly impressive number of Pleomothra, and Speleonectes), are restricted to anchialine caves aquatic environments (freshwater, brackish, marine), some spe- in the Bahamas, the Caicos Islands, Cuba, the Yucata´n Peninsula cies have become successful on land as well (e.g. isopods). Crusta- (Mexico), the Canary Islands, and the Cape Range Peninsula ceans have a chitinous exoskeleton impregnated with calcium (Western Australia). These small (up to 45 mm total length), carbonate, with three major body divisions: the cephalon, colourless, blind, elongate, centipede-like predators are found in 1מ Ͻ thorax, and abdomen, and they possess paired antennules, anten- their highest densities in oxygen-deficient waters ( 1mgl ), nae, mandibles, and maxillae. and are often found associated with other stygobitic crustaceans Not only have crustaceans been successful in epigean (above- such as caridean shrimps, cirolanid isopods, haziid amphipods, ground) habitats, but they have also moved into the hypogean mysids, ostracods, and thermosbaenaceans. (below-ground) realm, with six classes of crustaceans being rec- Class Copepoda ognized as inhabiting cave and other hypogean environments. (See also Crustacea: Copepoda.) Copepods are a large and di- Additionally, anchialine and interstitial habitats (although many verse group of crustaceans, and are the dominant forms of marine of the latter are not actually associated with karst landforms) plankton. Presently, more than 14 000 species are placed in harbour troglomorphic crustaceans. approximately 2300 genera in 210 families, yet the majority Like many other cavernicoles, many crustaceans are stygobites of subterranean species are placed in the following six orders: (aquatic obligate cavernicoles), while a few are troglobites (terres- Platycopioida and Misophrioida (occur in anchialine habitats), trial obligate cavernicoles). Both groups exhibit various morpho- Gelyelloida (found in caves in France and Switzerland), Cala- logical, physiological, and behavioural adaptations to living in noida, Cyclopoida, and Harpacticoida. Stygobitic species origi- a dark spelean environment where food is in short supply. Their nated from surface, marine, and freshwater ancestors and reached adaptations include reduction or loss of pigments and eyes, at- different groundwater habitats mostly through interstitial and tenuated appendages, and lowered metabolic rates. crevicular or karst routes. It is widely accepted that most obligate cavenicoles (including Calanoid copepods are mainly planktonic filter-feeders, rep- those other than crustaceans) evolved from epigean ancestors resented by some 2300 species, yet fewer than 20 are known with some degree of pre-adaptation to living in hypogean envi- from subterranean waters in a wide distribution ranging from ronments and are thought to have evolved by either natural the Americas to Madagascar and southeastern China. The cyclo- selection or by neutral mutation and genetic drift. poids (Figure 1b) are a poorly studied group, with approximately The six classes of crustaceans with subterranean representa- 150 species recognized from various caves, wells, anchialine habi- tives are Mystacocarida, Branchiopoda, Remipedia, Copepoda, tats, and groundwater interstices. These characteristically blind Ostracoda, and Malacostraca. The primitive Class Mystacocar- crustaceans lack pigments and are known from North and South ida is a meiobenthic group restricted to interstitial waters of America, Asia, Africa, Europe, and Madagascar. The harpacti- intertidal sand beaches and subtidal sand substrates. It is most coids (Figure 1c) are represented by nearly 3000 species assigned closely related to the Copepoda, and less than 20 species and to 40 families, at least 10 of which have stygobiont species. They subspecies are known from Africa, Europe, North and South are widely distributed in caves and various interstitial habitats, America, and Australia. Because mystacocarids are not known as well as in anchialine habitats. These vermiform crustaceans from karstic settings, there will be no further discussion here of can be observed scraping food from various substrates rather this group. Discussion of the remaining five classes of crustaceans than filtering water. follows. (The classes Copepoda and Ostracoda have their own entries in this Encyclopedia, as do three orders—Amphipoda, Class Ostracoda Isopoda, and Syncarida—of the Class Malacostraca.) (See also Crustacea: Ostracoda.) These bivalve crustaceans are fairly successful, being known from virtually all aquatic habitats, Class Branchiopoda but mostly from the marine environment. Some 5700 benthic Only the subclass Diplostraca includes species inhabiting subter- and planktonic species are recognized and more than 300 are ranean habitats (the hyporheos—or transition zone between endemic to subterranean waters, many assigned to the Order streams and groundwater, phreatic zone, caves). Although the Podocopida. Although some species are known only from caves Conchostraca (clam shrimps) and Cladocera (water fleas) are (e.g. Candona jeanneli in Marengo Cave, Indiana), most subter- included in this subclass, only the latter order has hypogean ranean forms have been observed in springs, interstitial waters, representatives, with fewer than 100 of the approximately 450 and anchialine habitats (Figure 1d). Stygobites are reported from recognized species occupying subterranean waters. These are Afghanistan, Africa, Bahamas, Bermuda, Canary Islands, Cen- small (0.2–2 mm), are laterally compressed, and there are only tral and Southern Europe, India, Jamaica, Japan, Java and West-

5603$$0C36 04-01-03 06:51:51 256 CRUSTACEA

Crustacea: Figure 1. Line drawings of dorsal (d) and lateral (l) views of representative stygobiont crustaceans: a. Remipedia (d) Speleonectes lucayensis from the Bahamas (after Hobbs, 2000; total length 19.8 mm); b. cyclopoid copepod (d) Kieferiella delamarei from France (after Hobbs, 2000; length 740 ␮m); c. harpacticoid copepod (d) Novocrinia trifida from Belize (after Huys and Iliffe, 1998; length 505 ␮m); d. thaumatocyprid ostracod (l) Danielopolina wilkensi from the Canary Islands (after Kornicker and Iliffe, 1995; length 0.41 mm). ern Malaysia, Mexico, North, Central, and South America, and (or with greatly reduced eyes), stygobites that evolved from shal- South Korea. low-marine ancestors and moved into anchialine habitats, caves, springs, thermal springs, wells, and occupy freshwater and saline Class Malacostraca environments. The group is widespread (found in Australia, the Clearly this is the largest class of crustaceans, with approximately Bahamas, Cambodia, Costa Rica, Croatia, Cuba, France, 23 000 species placed in six superorders, four of which contain Greece, Haiti, Italy, Lanzarote, Mallorca, Mexico, Morocco, hypogean species. The Superorder Syncarida (see Crustacea: Puerto Rico, Sicily, Spain, United States, and the Virgin Islands) Syncarida) is a poorly studied, freshwater group which is divided and consists of at least 34 species assigned to six genera in two into three orders, all of which share the absence of a carapace families. or cephalic shield. The Order Anaspidacea (Figure 2a) is known The Superorder Peracarida consists of eight orders, six of only from Australia, including the island of Tasmania, and occu- which have known subterranean species. Common characters pies a variety of aquatic habitats, including springs and caves, of this group include a carapace that is never fused to all the with one family (Psammaspididae) that is exclusively stygobitic. thoracomeres, although the carapace in isopods and amphipods The Order Stygocaridacea (Figure 2b) occupies interstitial waters secondarily has been lost, the first pair of thoracopods (thoracic in epigean and hypogean environments in New Zealand and somites with a pair of appendages) is modified as a pair of maxil- South America. Fewer than 10 species are assigned to four gen- lipeds, the females have a brood pouch, and the pleopods lack era. The Order Bathynellacea (Figure 2c) has the greatest species an appendix interna (a slender appendage of the endopod). The richness of the three orders, with approximately 150 species rec- Order Mysidacea is a diverse group of crustaceans with more ognized from interstitial epigean, well, and cave habitats. This than 1000 species widely distributed in marine, freshwater, and ancient, relict group is known from Africa, Asia, Australia, Eu- groundwater habitats. Stygobitic mysids (Figure 3a) occur in rope, Japan, Madagascar, New Zealand, and North and South anchialine habitats, wells, and blue holes in Africa (Kenya, Zan- America. zibar) the Bahamas, the Balearic Islands, Bermuda, Bosnia / Her- The Superorder Pancarida is represented by the Order Ther- cegovina, Canary Islands, Cuba, India, Jamaica, the Lesser Antil- mosbaenacea (Figure 2d). These are small (4 mm or less), eyeless les, Mexico, Puerto Rico, southern Italy, and the Turks and

Crustacea: Figure 2. Line drawings of dorsal (d) and lateral (l) views of representative stygobiont crustaceans: a. anaspidacean syncarid (l) Psammaspides williamsi from Australia (after Hobbs, 2000; length 6.7 mm); b. stygocaridacean syncarid (l) Stygocaris sp. (after Hobbs, 2000; 500 ␮m); c. bathynellacean syncarid (l) Notobathynella williamsi from Australia (after Hobbs, 2000; length 1.46 mm); d. Thermosbaenacea (d) Monodella relicta from Israel (after Botosaneanu, 1986; length 2.6 mm).

5603$$0C36 04-01-03 06:51:51 CRUSTACEA 257

Crustacea: Figure 3. Line drawings of dorsal (d) and lateral (l) views of representative stygobiont crustaceans: a. Mysidacea (d) Speleomysis longipes from India (after Hobbs, 2000; length 5.8 mm); b. speleogriphacean peracarid (l) Spelaeogriphus lepidops from South Africa (after Hobbs, 2000; length 6.0 mm); c. mictacean peracarid (l) Mictocaris halope from Bermuda (after Hobbs, 2000; length 3.0 mm); d. boshusacean peracarid (d) Thetispelecaris remex from the Bahamas (after Hobbs, 2000; length 1.2 mm).

Caicos islands. At least 28 stygobites, most of which are endem- The Order Isopoda (see Crustacea: Isopoda: Oniscidea) has ics, are recognized and the distribution of most species suggests more than 11 000 described terrestrial and aquatic species and that the majority colonized groundwaters due to stranding and is widely distributed across most habitats. These crustaceans lack uplifting of their marine ancestors resulting from the regressions a carapace, are dorsoventrally compressed, and have pleopods of the Tethys and Mediterranean seas. Other taxa have invaded modified for respiration. Eight of eleven suborders have subterra- groundwaters more recently and are stygophiles. nean representatives: Anthuridea, Asellota, Calabozoidea, Cy- The Order Tanaidacea is represented by some 850 marine mothoidea, Microcerberidea, Oniscidea, Phreatoicidea, and benthic species. Only three species are characteristic inhabitants Sphaeromatidea. Most anthurideans are marine, but approxi- of marine caves in Bermuda, Koror Island (Palau), and Niue mately 20 species occur in interstitial sediments of rivers, Island (South Pacific) and it is unclear whether or not any of beaches, wells, anchialine habitats, and caves in the Canary Is- these species are obligate cavernicoles. lands, the Caribbean and Indian Ocean islands, Mexico, and The Order Cosinzeneacea was recently erected to house the South America. The Asellota (Figure 4a) is a diverse group that stygobitic suborders Spelaeogriphacea and Mictacea. The Subor- is divided into five superfamilies. These isopods inhabit ground- der Spelaeogriphacea is represented by three monotypic genera: waters of caves, wells, springs, thermal springs, the hyporheos, Spelaeogriphus lepidops (South Africa—Figure 3b), Potiicoara and anchialine habitats in Africa, the Bahamas, Belize, Bonaire, brasiliensis (Brazil), and Mangkurtu mityuula (Western Austra- Cuba, Curac¸ao, Europe, the Galapagos Islands, India, Indonesia, lia). All have a small saddle-like carapace which is fused with the Japan, Madagascar, Malaysia, North and Central America, and first thoracic somite and, anteriorly, is produced into a broadly Polynesia. The Calabozoidea is monotypic, restricted to a phre- triangular rostrum. The thoracopods and pleopods are reduced atic system in northern Venezuela, and this stygobite is closely and the abdomen is elongate, often exceeding half the total body related to the Asellota. Subterranean representatives of the cymo- length. The Suborder Mictacea is represented by Mictocaris ha- thoideans are restricted to the mostly marine family Cirolanidae lope (Figure 3c), known from marine caves on Bermuda. This (Figure 4b), of which approximately 50 are stygobites. Micro- non-predatory crustacean swims, rests, or walks on the substrata cerberideans are slender, blind, pigmentless stygobites of which of anchialine caves. about 60 species occur in interstices of marine beaches, wells, The Order Bochusacea was recently erected to accommodate and caves near coastal areas of southern Africa, southeastern Asia, three marine species belonging to the family Hirsutiidae, two of the Caribbean, Indian Ocean islands, Japan, and the Mediterra- which are deep-water marine forms, while Thetispelecaris remex nean. Oniscideans (see Crustacea: Isopoda: Oniscidea) are (Figure 3d) is a stygobite, inhabiting anchialine and submarine mostly terrestrial, although some stygobitic species (Trichonisci- caves in the Bahamas. dae) inhabit cave waters. Although some 3500 species are known,

Crustacea: Figure 4. Line drawings of dorsal (d) and lateral (l) views of representative stygobitic crustaceans: a. asellid isopod (d) Proasellus valdensis from France (after Hobbs, 2000; length 8.0 mm); b. cirolanid isopod (d) Anopsilana conditoria from the Philippines (after Bruce & Iliffe, 1992; length 2.9 mm); c. amphipod peracarid (l) Stygobromus exilis from Kentucky, United States (after Hobbs, 2000; length 6.0 mm).

5603$$0C36 04-01-03 06:51:51 258 CRUSTACEA only 14 families have subterranean representatives and are global tropical and tropical latitudes. The global Infraorder Caridea in their distribution. The stygobiont Phreatoicidea is the most (shrimps) is quite diverse, with nearly 2000 species, yet only ancient group of isopods, dating back to the Carboniferous. about 137 species dwell in springs, wells, caves, blue holes, ceno- Prior to the breakup of Gondwana they invaded freshwater habi- tes, and anchialine habitats. They are concentrated in tropical tats, and currently most species are epigean, although some are latitudes but are known from Africa, Ascension Island, the Car- known from wells and caves in Australia, India, New Zealand, ibbean and western Atlantic islands, Georgia, India, the Indian and southern Africa. The sphaeromatideans are mostly marine Ocean islands, Indonesia, Japan, Madagascar, Melanesia, Mex- crustaceans, but approximately 36 are stygobites that are re- ico, Micronesia, the Middle East, Southern Europe, the United stricted to subterranean waters in Southern Europe. States, and Western Australia. A single stygophilic palinuran is The Order Amphipoda (see Crustacea: Amphipoda) is char- known from a sea cave in New Zealand; the stenopodideans are acterized as being laterally compressed, lacking a carapace, and represented by a stenoxene from a lava tube on Lanzarote, and being generally an aquatic group consisting of more than 6700 the thalassinidean is known from a cave on Acklins Island, Ba- species placed in three suborders: Caprellidea, Gammaridea, and hamas. Hyperiidea. Stygobitic amphipods are known only from the HORTON H. HOBBS III large Suborder Gammaridea (Ͼ5700 species) and the approxi- Works Cited mately 750 troglomorphic species are assigned to about 160 genera. Although there are more than 30 families, the Bogidielli- Botosaneanu, L. (editor) 1986. Stygofauna Mundi, A Faunistic, dae, Crangonyctidae (Figure 4c), Hadziidae, and Niphargidae Distributional, and Ecological Synthesis of the World Fauna demonstrate the greatest biodiversity. They are found virtually Inhabiting Subterranean Waters (Including the Marine Interstitial), in all parts of the globe with appropriate habitats, but Central Leiden: Brill and Southern Europe, the Mediterranean region, eastern and Bruce, N.L. & Iliffe, T.M. 1992. Anopsilana conditoria,anew species of anchialine troglobitic cirolanid isopod (Crustacea) from southern North America, and the Caribbean house the largest the Philippines. Stygologia, 7(4): 225–30 taxonomic diversity of stygobitic amphipods. Hobbs III, H.H. 2000. Crustacea. In Subterranean Ecosystems, edited The Superorder Eucarida (see Crustacea: Decapoda) is char- by H. Wilkens, D.C. Culver & W.F. Humphreys, Amsterdam acterized by a cephalothorax (carapace fused to all thoracomeres) and New York: Elsevier and represents the most highly evolved group of malacostracans. Huys, R. & Iliffe, T.M. 1998. Novocriniidae, a new family of Three orders are assigned to this superorder but only the Deca- harpacticoid copepods from anchihaline caves in Belize. Zoologica poda occupy subterranean environments. Decapods are the larg- Scripta, 27(1): 1–15 est and most diverse order (nearly 10 000 species) and possess Kornicker, L.S. & Iliffe, T.M. 1995. Ostracoda (Halocypridina, three pairs of maxillipeds and five pairs of functional pereiopods Cladocopina) from an anchialine lava tube in Lanzarote, Canary (hence the name Decapoda). Although widespread in distribu- Islands. Smithsonian Contributions to Zoology, 568: 1–32 tion, the subterranean species are concentrated in Africa, Central Further Reading and North America, and the Philippines and are divided among Culver, D.C. & Wilkens, H. 2000. Critical review of the relevant seven infraorders: Anomura, Astacidea, Brachyura, Caridea, Pali- theories of the evolution of subterranean animals. In Subterranean nura, Stenopodidea, and Thalassinidea (the last three are not Ecosystems, edited by H. Wilkens, D.C. Culver & W.F. stygobites). The Anomura include crabs such as the marine her- Humphreys, Amsterdam and New York: Elsevier mit, porcelain, mole, and sand crabs, yet subterranean species are Gutu, M. & Iliffe, T.M. 1998. Description of a new hirsutiid (n.g., mostly known from two families: Aeglidae (Aegla cavernicola— n.sp.) and reassignment of this family from Order Mictacea to Brazil) and Galatheidae (Munidopsis polymorpha—Lanzarote). the new Order Bochusacea (Crustacea, Peracarida). Travaux du Assigned to the Infraorder Astacidea are approximately 900 spe- Muse´um d’Histoire naturelle Grigore Antipa, 40: 93–120 cies of crayfishes and chelate lobsters. Only crayfishes have in- Juberthie, C. & Decu, V. (editors) 1994. Encyclopaedia Biospeologica, vaded subterranean waters, with 39 stygobitic species assigned 2 vols, Moulis and Bucharest: Socie´te´ de Biospe´ologie Wagner, H.P. 1994. A monographic review of the Thermosbaenacea to four genera (Cambarus, Orconectes, Procambarus, and Troglo- (Crustacea: Peracarida): a study on their morphology, taxonomy, cambarus)inNorth America and Cuba. Brachyurans (“true phylogeny and biogeography. Zoologische Verhandelingen (Leiden), crabs”) are dorsoventrally compressed crustaceans, with about 1994: 3–338 4500 known species, of which only approximately 96 dwell in Yager, J. 1981. Remipedia, a new class of Crustacea from a marine hypogean waters. They are widely distributed primarily in sub- cave in the Bahamas. Journal of Crustacean Biology,1:328–33

CRUSTACEA: AMPHIPODA Amphipods belong to the arthropod subphylum Crustacea and Caprellidea, Hyperiidea, and Ingolfiellidea. However, the latter the order Amphipoda. They typically range in size from 2 to 50 may be highly specialized gammarideans that do not merit recog- mm, although a few are larger. Amphipods are common in nition as a suborder. Gammaridea, with more than 5500 de- aquatic ecosystems throughout many parts of the world, where scribed species, is the largest amphipod suborder and contains they inhabit marine, brackish, and freshwater environments. A all of the freshwater and subterranean taxa. Approximately 21 few species also live in terrestrial ecosystems. The order Amphi- superfamily groups, 95 families (or family groups) and more poda, which contains approximately 7000 described species, is than 1000 genera are classified in this suborder (Holsinger, divided into three and sometimes four suborders: Gammaridea, 1994).

5603$$0C37 04-01-03 06:55:29