Crymostygidae, a new family of subterranean freshwater ...

JOURNAL OF NATURAL HISTORY, 2004, 38, 1881–1894

Crymostygidae, a new family of subterranean freshwater gammaridean amphipods (Crustacea) recorded from subarctic Europe ´ NSSON{ and J. SVAVARSSON{ B. K. KRISTJA {Holar College, 551 Skagafjo¨rður, Iceland; e-mail: [email protected] {Institute of Biology, University of Iceland, Grensa´svegur 12, 108 Reykjavı´k, Iceland (Accepted 16 June 2003) Crymostygidae, a new family of gammaridean amphipods (Crustacea), is described from Iceland. The family is based on a new species and genus, Crymostygius thingvallensis, found in spring inlets feeding Lake Thingvallavatn, south-west Iceland. This is the first report of a stygobiont freshwater amphipod from Iceland and the northern-most report of a stygobiont species in Europe. The species apparently survived Pliocene and Pleistocene glaciations in the groundwater of a porous lava and may have persisted in Iceland for several million years. KEYWORDS: Crymostygius thingvallensis, Iceland, stygobiont, groundwater, Iceage survival, Crymostygidae, Crangonyctoidea.

Introduction Amphipods (Crustacea) are among the most species-rich peracarid groups with over 7000 known species and among the most diverse subterranean animal groups, with close to 1000 known stygobitic species (Sket, 1999). The highest diversity of subterranean amphipods is in southern and central Europe, in eastern and southern North America, and in the West Indies (Holsinger, 1993; Sket, 1999). Despite this high diversity, stygobiont amphipods have not been recorded in subarctic or arctic areas in Europe or Greenland, but have been reported from subarctic Alaska and Siberia (Holsinger, 1986). In 1998, a specimen of amphipod was collected at spring inlets in Lake Thingvallavatn, south-west Iceland (64‡14’N, 21‡03’W), using electric fishing gear, while collecting three-spined sticklebacks (Gasterosteus aculeatus L.). A second and a third specimen were collected later (2000, 2003) at the same location. This is the first report of a stygobiont amphipod in Iceland. Furthermore, this is the first record of a strictly freshwater amphipod in Iceland and the first report of a stygobiont amphipod in subarctic Europe. The species collected has morphological affinities to the crangonyctoidean families Crangonyctidae Bousfield, 1977, Journal of Natural History ISSN 0022-2933 print/ISSN 1464-5262 online # 2004 Taylor & Francis Ltd http://www.tandf.co.uk/journals DOI: 10.1080/00222930310001597295

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B. K. Kristjańsson and J. Svavarsson

Allocrangonyctidae Holsinger, 1989 and Pseudocrangonyctidae Holsinger, 1989. The new species, however, has a combination of characters that distinguish it from the species known within these families. A new family is erected to accommodate the new species. The material is deposited at the Icelandic Museum of Natural History (IMNH), Reykjavı´k, Iceland. Taxonomy CRYMOSTYGIDAE, new family Diagnosis. Female body large, long and slender, unpigmented. Eyes rudimentary. Pleonites with several fine setae on posterior margin. Uronites 1 and 2 with posterodorsal clusters of differently sized setae; a single posterodorsal spine in setae cluster on uronites 1–3. Interantennal lobe of head evenly rounded anteriorly, inferior antennal sinus moderately deep. Coxae shallow, contiguous, posterior margin of coxa 4 without excavation. Distoposterior corners of pleonal plates rounded. Antennae 1 longer than antennae 2, accessory flagellum threesegmented. Antennae without calceoli. Mandibular palp present, molar pointed, truncated distally, bearing long single seta. Maxilla 1 with inner plate ovate, outer plate apically with about 17 spines, medial margin of spines with 19–24 denticles, palp two-segmented. Maxilla 2 with both plates with similar armature, outer plate with single group of distal setae. Maxilliped with outer plate with about six blade spines subapically; apically about six plumose setae distally, about 16 naked setae on inner margin. Inner plate with five blade-like spines and six plumose setae on apical and subapical inner margin. Propodus of gnathopods relatively large (crangonyctid-like), subchelate, propod of gnathopod 2 larger and more slender than propod of gnathopod 1, palm long, oblique, armed with single row of distally notched spines. Pereopods 3 and 4 normal, subequal, 5–7 increasing in overall length posteriorly, dactyls of pereopods 3–7 with few to several posterior marginal setae. Simple coxal gills on gnathopod 2 and pereopods 3–6. Pair of sternal gills on pereonites 3–7. Brood-plates present on pereopods 2–5, brood-plates long and slender. Pleopods normal, subequally biramous, peduncles with two coupling hooks each. Uropods 1 and 2 biramous. Uropod 3 with vestigial inner ramus, outer ramus two-segmented, second segment small. Telson slightly longer than wide, apex truncated, with two apical spines. Etymology. The name is drawn from the Greek word crymos meaning ice or frost and the name of the river Styx, referring to subterranean waters, indicating that the family encompasses species that have survived glaciations in subterranean waters. Remarks. The family is composed of only a single genus and species. The family falls within the superfamily Crangonyctoidea, but differs in many important characteristics from the families Pseudocrangonyctidae Holsinger, 1989, Allocrangonyctidae Holsinger, 1989 and Crangonyctidae Bousfield, 1977 (Bousfield, 1977; Holsinger, 1989). The new family shares several characters with the monotypic family Allocrangonyctidae from North America, such as the presence of dorsal spines on the uronites, two-segmented outer ramus of the third uropod and posterior

Crymostygidae, a new family of amphipods

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marginal spines on the dactylus of the posterior pereopods. There are, however, important differences between the new family and the Allocrangonyctidae, the latter having a bilobed coxal gill on gnathopod 2, two-segmented accessory flagellum, non-serrate spines on the apex of the outer plate of maxilla 1, inner plate of maxilla 1 with one apical seta and apical margin of the outer plate of maxilla 2 with two distinct groups of setae, and lacking sternal gills. Furthermore, the gnathopod 1 of the Allocrangonyctidae is Niphargus-like. The new family resembles further the north-east Asian family Pseudocrangonyctidae in several aspects, such as having spines dorsally on the uronites, in the general shape of the habitus, shape of the gnathopods, having dactylus of the gnathopods with a row of blade-like processes, structure of the mandible, and in having two-segmented outer ramus and a vestigial inner ramus. Important differences between the new family and the Pseudocrangonyctidae are seen in the presence of the three-segmented accessory flagellum of the present species, in the structure of the spines of maxilla 1 and 2, such as having an outer plate of maxilla 1 apically with about 17 spines, in the absence of rastellate setae on the gnathopods and in the presence of only a single row of distally notched spines on the palms of the propods of the gnathopods. Additionally, the present species has a vestigial inner ramus of uropod 3, which is absent from the Pseudocrangonyctidae. The new family shows resemblance to a few of the genera of the large holarctic family Crangonyctidae in body shape and in structure of the mouth parts and the uropods. There are, however, important differences that exclude the species from the Crangonyctidae, such as the three-segmented accessory flagellum of the first antennae and the presence of dorsal setae and spines on the uronites. Type genus. Crymostygius new genus, by monotypy. Crymostygius gen. nov. Diagnosis. As for the family. Type species. Crymostygius thingvallensis new species, by monotypy. Crymostygius thingvallensis sp. nov. (figures 1–6) HOLOTYPE: female, 18 mm, 7 June 1998, Vatnsvik (64‡14’46@N, 21‡03’19@W), Thingvallavatn, Iceland (figure 7), groundwater inflow, electric fishing, coll. B. K. Kristjańsson, IMNH 2003.06.17.1. PARATYPES: female, 22 mm, 9 August 2000, Vatnsvik (64‡14’46@N, 21‡03’19@W), Thingvallavatn, Iceland, groundwater outflow, electric fishing, coll. B. K. ´. O ´ lafsdo´ttir, preserved in alcohol, IMNH 2003.06.17.2. Kristjańsson and G. A Juvenile, 13 mm, 30 June 2003, Vatnsvik (64‡14’46@N, 21‡03’19@W), Thingvallavatn, Iceland, groundwater inflow, electric fishing, coll. B. K. Kristjańsson, IMNH 2003.07.03.1. Diagnosis. As for the genus. Description. Adult body length 18–22 mm (figure 1). Body long and slender, unpigmented. Indication of eye pigment. Pleonites with several fine setae on posterior margin. Uronites unfused, uronites 1 and 2 with posterodorsal clusters of differently sized setae, single posterodorsal seta in each setae cluster on uronites 1, 2 and on uronite 3 (female paratype only with spines in cluster on uronite 2).

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FIG. 1.


Crymostygius thingvallensis, n. sp. Female holotype, 18 mm. Habitus. Scale: 2 mm.

Interantennal lobe of head evenly rounded anteriorly, inferior antennal sinus moderately deep (figure 1C). Coxae shallow, contiguous, posterior margin of coxa 4 without excavation. Distoposterior corners of pleonal plates rounded. Antenna 1 (figure 2A) 43–53% length of body, about 125% longer than antenna 2; peduncle segment 1 80% of combined length of segments 2 and 3; primary flagellum with about 30 segments; accessory flagellum three-segmented, terminal segment short.


FIG. 2.

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Crymostygius thingvallensis, n. sp. Female holotype, 18 mm. (A) Antenna 1 (accessory flagellum enlarged); (B) antenna 2; (C) upper lip; (D) left mandible (lacina mobilis, incisor and molar process enlarged); (E) right mandibular palp; (F) lower lip; (G) maxilla 1; (H) maxilla 2.

Antenna 2 (figure 2B) with peduncular segment 5 subequal to segment 4, 46% of length of flagellum. Flagellum with 14 segments. Upper lip (figure 2C) evenly rounded, fine setae on distal margin. Mandible (figure 2D) well developed. Left lacina mobilis seven-dentate, incisor five-dentate, nine large spines and some small in spine row; molar pointed, truncated distally, one long seta subapically. Palp with three segments (figure 2E;

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FIG. 3.


Crymostygius thingvallensis, n. sp. Female holotype, 18 mm. (A) Maxilliped; (B) outer plate of maxilliped; (C) inner plate of maxilliped; (D) gnathopod 1; (E) posterior margin of dactylus of gnathopod 1; (F) palmar margin propodus of gnathopod 1, showing bifid spines and medial setae; (G) gnathopod 2.

segment segment segment plumose

3 missing in left mandible of holotype, second segment regenerating), 2 with 15 plumose setae on lateral margin, 72% of length of segment 3; 3 with four or five long plumose E-setae, row of more than 35 short D-setae, pair of long B-setae.


FIG. 4.

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Crymostygius thingvallensis, n. sp. Female holotype, 18 mm. (A) Pereopod 3; (B) pereopod 4; (C) dactylus of pereopod 4; (D) pereopod 5; (E) propodus and dactylus of pereopod 5.

Lower lip (figure 2F, slightly damaged, inner lobes presumably missing) with outer lobes evenly rounded; fine setae on distal margin. Maxilla 1 (figure 2G): inner plate ovate, medial row of six plumose setae, small setae apically. Outer plate apically with about 17 spines, medial margin of spines with 19–24 denticles. Palp two-segmented, segment 2 apically and subapically with short plumose setae and six simple setae, one longer plumose seta laterally. Maxilla 2 (figure 2H): both plates with similar armature, larger setae on inner plate, outer plate with single group of distal setae. Maxilliped (figure 3A): outer plate (figure 3B) with about six blade spines subapically; apically about six plumose setae distally, about 16 naked setae on inner margin. Inner plate (figure 3C) with five blade-like spines and six plumose setae on apical and subapical inner margin. Dactylus with fairly long, uncurved nail. Gnathopod 1 (figure 3D) stout; coxal plate longer than wide, with several setae anteriorly and distally; posterior margin of basis with clusters of long setae; basis

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FIG. 5.


Crymostygius thingvallensis, n. sp. Female holotype, 18 mm. (A) Pereopod 6; (B) pereopod 7; (C) dactylus of pereopod 7.


FIG. 6.

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Crymostygius thingvallensis, n. sp. (A–G) Female holotype, 18 mm; (H) female paratype, 22 mm. (A) Pleopod 1; (B) coupling spines of pleopod 1; (C) uropod 1; (D) uropod 2; (E) uropod 3 (second segment of outer ramus missing); (F) inner ramus of uropod 3; (G) outline of telson (apical setae and spines missing from holotype); (H) uronites 1–3, telson and uropods 2 and 3.

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FIG. 7.


Location of Iceland and Lake Thingvallavatn. The large recent glaciers, Langjo¨kull, Hofsjo¨kull and Vatnajo¨kull, are shown.

and merus posterodistally fringed with slender setae; ischium posteriorly with four rows of marginal setae; carpus evenly convex posterodistally, eight rows of marginal setae; propodus ovoid, much longer than carpus, palmar margin slightly oblique, no distinct angle; palmar margin with about 19 bifid spines (figure 3F) and rows with few setae; dactylus about 70% of propodus length; dactylus with row of blade-like processes on posterior margin (figure 3E); unguis about 33% of dactylus length. Gnathopod 2 (figure 3G, gills not shown) stout, longer than gnathopod 1; coxal


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plate longer than wide, with several setae anteriorly and distally; basis longer than basis of gnathopod 1, posterior margin of basis with seven clusters of long setae; basis and merus posterodistally fringed with slender setae; ischium posteriorly with two rows of marginal setae; carpus angular posterodistally, seven rows of marginal setae, posterodistally numerous setae; propodus longer than propodus of gnathopod 1; much longer than carpus, palmar margin slightly oblique, no distinct angle; palmar margin with about 16 bifid spines on distal part of margin; eight rows with several setae proximally, few setae on distal margin, medio-anteriorly five rows of setae; dactylus about 58% of propodus length; dactylus with row of blade-like processes on posterior margin; unguis about 31% of dactylus length. Pereopods 3 and 4 (figure 4A, B) slender, subequal in length; coxal plate longer than wide, with several setae anteriorly and distally. Basis slender; anteriorly, posteriorly and medially fringed with slender setae; dactylus about 35% of propodus length, several fine setae on posterior margin of dactylus (figure 4C). Pereopods 5–7 (figures 4D, 5A, B) longer than pereopods 3 and 4, increasing in length towards posterior end. Basis slender, several fine setae on posterior margin of dactylus, increasing in numbers on posterior pereopods (figures 4E, 5C). Stalked, club-shaped coxal gills present on gnathopod 2 and pereopods 3–6. Pair of lateral sternal gills on pereonites 3–7. Brood-plates present on pereopods 2–5, long and slender (figures 3, 4). Pleopods 1–3 similar, biramous, unmodified, peduncle bearing two coupling spines. Pleopod 1 (figure 6A, B) outer ramus with at least 16 free segments and few fused segments proximally, inner ramus with at least 13 segments and few fused segments proximally. Similar segmentation on posterior pleopods. Uropod 1 (figure 6C) slender, with about 11 spines on dorsal surface. Inner ramus with five apical spines, seven spines on dorsal surface. Outer ramus with four apical spines and about nine spines on dorsal surface. Uropod 2 (figure 6D) with two spines on dorsolateral margin, one seta dorsodistally, four setae on dorsomedial margin. Inner ramus slightly longer than outer ramus, about as long as peduncle, with five apical spines and four spines on dorsal surface. Outer ramus with four apical spines and six spines on dorsal surface. Uropod 3 (figure 6E, F, H) approximately 11.6% of body length. Peduncle small, one spine ventrodistally. Inner ramus vestigial, about as long as penduncle, 10% of length of outer ramus (figure 6F). Inner ramus distally with four small setae. Outer ramus two-segmented, with several apical spines on first segment, clusters of spines on lateral and medial margins; second segment with fine setae apically (figure 6H). Telson (figure 6G) longer than broad, apical margin truncated with indication of small notch, apparently two to three spines and setae on apical lobes (female paratype with two setae and single seta respectively on each apical lobe). Etymology. The species is named after the place Thingvellir (Þingvellir in Icelandic). The name means meeting (þing) and fields (vellir) and the Vikings came to þingvalla (thingvalla). In 930–1262 the Viking-Age settlers of Iceland established a remarkable society with an annual national assembly, the Althingi, as its most important institution, which met at Thingvellir. The gender is masculine. Remarks. Only the female is known of this species. The species was collected at a spring inlet in Thingvallavatn. The lake, its formation, geology and its limnic ecosystem have been extensively studied (Jońasson, 1992). The lake is

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about 90% fed by groundwater (Adalsteinsson et al., 1992). Around 20% of the groundwater inflow occurs at and nearby Vatnsvik. In the Vatnsvik area the groundwater is characterized by stability in ´ lafsson, 1992). The groundwater originates mainly temperature around 3‡C (O from the ice cap of glacier Langjo¨kull (figure 7) and flows from its origin under the glacier towards the springs in less than 10 years (see discussion in Sveinbjo¨rnsdo´ttir and Johnsen, 1992). The water flows through Eldborgir lava which has been dated at the age of 9130¡260 years (Kjartansson, 1964; Sæmundsson, 1992). Discussion Though being very abundant in many parts of the world, subterranean amphipods have not been recorded before in subarctic or arctic areas in Europe. The northern-most records in Europe are from southern England and Ireland (Costello, 1993). In North America stygobiont amphipods reach as far north as the Great Lakes, British Columbia and Alaska, and stygobiont amphipods have been recorded from Siberia (Holsinger, 1986). The discovery of an endemic genus and family of stygobiont, freshwater amphipod in Iceland is of considerable biogeographical interest. It is especially noteworthy in light of the remote location of the island and its glaciation history. Iceland was fully covered by glaciers for prolonged periods, beginning in the Miocene, with a maximum at around 2.6 million years ago, ending only some 10–12 000 years ago (Geirsdo´ttir and Eirı´ksson, 1994). Consequently, the fauna and flora is generally considered to have arrived in Iceland after the last glacial epoch (Coope, 1986; Sadler, 1999), although some plants may have survived on nunataks during periods of glaciations (Rundgren and Ingo´lfsson, 1999). No other endemic species, except some plant ‘microspecies’, are known from the island. Prior to the glaciations Iceland had presumably a warm climate and deciduous forests (Sı´monarson, 1979). The oldest Icelandic animal fossil is a hickory aphid dating from 6.7 to 16 million years ago, closely resembling the species Longistigma caryae Harris, 1841, which lives presently in deciduous forests in North America (Heie and Friedrich, 1971). Stygobiont amphipods have been found on many oceanic islands in the Atlantic Ocean (Stock, 1993). Due to their limited possibilities of dispersal, their distribution is usually considered due to vicariance (Holsinger, 1991, 1993; Stock, 1993). The origin of the species is usually traced to the opening of the Atlantic Ocean and the break-up of the Tethys Sea. This is supported by the distribution of many species. The endemic Crymostygius thingvallensis has undoubtedly survived the Pliocene and Pleistocene glaciations in the groundwater of Iceland. The groundwater may continue to flow through the ground despite an overlying glacier. Young lava in particular has a high porosity and eruptions (subglacial and non-subglacial) were frequent in Iceland’s geological history. Also, in Iceland geothermal activity is substantial, causing periodical melting of glaciers. Subglacial refugia have earlier been suggested for species of the genera Stygobromus and Bactrurus (Holsinger, 1981, 1986; Koenemann and Holsinger, 2001). On the basis of the distribution of B. mucronatus Koenemann and Holsinger (2001) provide solid argument for the species having survived glaciations in North America. It is still premature to discuss the possible origin of the present species. Affinity to the families Pseudocrangonyctidae, Allocrangonyctidae and Crangonyctidae indicates a freshwater origin and possibly a North American/Eurasian connection


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(sensu Holsinger, 1986, 1989; Notenboom, 1991). Such a connection is supported by the presence of a fossil aphid with North American affinity (Heie and Friedrich, 1971). Holsinger (1986, 1989) has suggested that the Allocrangonyctidae and the Crangonyctidae represent a very ancient group of amphipods, which probably originated on the Laurasian palaeocontinent prior to the separation of Eurasia and North America. Acknowledgements We wish to thank all those that assisted in many attempts to collect more specimens of the species. We thank John Holsinger, Agnar Ingo´lfsson, Niel L. Bruce and Svavar Hrafn Svavarsson for their valuable comments and advice. The Icelandic Research Council supported the study. References ADALSTEINSSON, H., JOŃASSON, P. M. and RIST, S., 1992, Physical characteristics of Thingvallavatn, Iceland, Oikos, 64, 121–135. BOUSFIELD, E. L., 1977, A new look at the systematics of gammaroidean amphipods of the world, Crustaceana, Supplement, 4, 282–316. COOPE, G. R., 1986, The invasion and colonization of the North Atlantic islands: a palaeoecological solution to a biogeographical problem, Philosophical Transactions of the Royal Society of London, Series B, 314, 619–635. COSTELLO, M., 1993, Biogeography of alien amphipods occurring in Ireland, and interactions with native species, Crustaceana, 65, 287–299. ´ . and EIRI´KSSON, J., 1994, Growth of an intermittent ice sheet in Iceland GEIRSDO´TTIR, A during the late Pliocene and early Pleistocene, Quartenary Research, 42, 115–130. HEIE, O. E. and FRIEDRICH, W. L., 1971, A fossil specimen of the North American hickory aphid (Longistigma caryae Harris), found in Tertiary deposits in Iceland, Entomologica Scandinavica, 2, 74–80. HOLSINGER, J. R., 1981, Stygobromus canadensis, a troglobite amphipod crustacean from Castleguard Cave, with remarks on the concept of glacial refugia, Proceedings of the 8th International Congress of Speleology, 1, 93–95. HOLSINGER, J. R., 1986, Zoogeographical patterns of North American subterranean amphipod crustaceans, in R. H. Gore and K. L. Heck (eds) Crustacean Biogeography, Crustacean Issues, 4, 85–106. HOLSINGER, J. R., 1989, Allocrangonyctidae and Pseudocrangonyctidae, two new families of Holarctic subterranean amphipod crustaceans (Gammaridea), with comments on their phylogenetic and zoogeographic relationships, Proceedings of the Biological Society of Washington, 102, 947–959. HOLSINGER, J. R., 1991, What can vicariance biogeographic models tell us about the distributional history of subterranean amphipods? Hydrobiologia, 223, 43–45. HOLSINGER, J. R., 1993, Biodiversity of subterranean amphipod crustaceans: global patterns and zoogeographic implications, Journal of Natural History, 27, 821–835. JOŃASSON, P. M., 1992, Thingvallavatn research history, Oikos, 64, 15–31. KJARTANSSON, G., 1964, 14C ages of some postglacial lavas in South-Iceland, Na´ttu´rufræðingurinn, 34, 101–113 (in Icelandic). KOENEMANN, S. and HOLSINGER, J. R., 2001, Systematics of the North American subterranean amphipod genus Bactrurus, Beaufortia, 51(1), 1–56. NOTENBOOM, J., 1991, Marine regressions and the evolution of groundwater dwelling amphipods (Crustacea), Journal of Biogeography, 18, 437–454. ´ LAFSSON, J., 1992, Chemical characteristics and trace elements of Thingvallavatn, Oikos, O 64, 151–161. ´ ., 1999, Plant survival in Iceland during periods of RUNDGREN, M. and INGO´LFSSON, O glaciation? Journal of Biogeography, 26, 387–396. SADLER, J. P., 1999, Biodiversity on oceanic islands: a palaeoecological assessment, Journal of Biogeography, 26, 75–87.

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SÆMUNDSSON, K., 1992, Geology of the Thingvallavatn area, Oikos, 64, 40–68. SI´MONARSON, L., 1979, On climatic changes in Iceland, Jo¨kull, 29, 44–46. SKET, B., 1999, The nature of biodiversity in hypogean waters and how it is endangered, Biodiversity and Conservation, 8, 1319–1338. STOCK, J. H., 1993, Some remarkable distribution pattern in stygobiont Amphipoda, Journal of Natural History, 27, 807–819. ´ . E. and JOHNSEN, S. J., 1992, Stable isotope study of the SVEINBJO¨RNSDO´TTIR, A Thingvallavatn area. Groundwater origin, age and evaporation models, Oikos, 64, 136–150.