Survey
* Your assessment is very important for improving the workof artificial intelligence, which forms the content of this project
* Your assessment is very important for improving the workof artificial intelligence, which forms the content of this project
AM. ZOOLOGIST, 8:327-353 (19G8). Transition from Water to Land in Amphipod Crustaceans DESMOND E. HURLEY New Zealand Oceanographic Institute, Wellington, New Zealand SYNOPSIS. Truly terrestrial Amphipoda are known solely in the Family Talitridae, the only family also found extensively in the supralittoral. Commonly, they are crytozoic inhabitants of the leafmold of tropical or southern cold-temperate forests. Except as recent introductions, they are absent from Europe and North America. There are a few records from Central America and the Caribbean. The success of the talitrids in colonizing the land is considered due to invasion of leafmold direct from supralittoral debris. Leafmold provides an insulated niche with sufficient food and moisture for colonization with little modification. Apart from possible loss of pleopods, adaptations appear merely to continue trends already present in littoral species. Present distribution can only partly be explained in terms of past geology. Leafmold species are derived from cosmopolitan supralittoral genera and may have arisen independently in different countries. Some widely-distributed species, e.g., Talitrus pacificus, may have been transported by man; accidental transplantation o£ terrestrial amphipods is known. The Amphipoda have not achieved the terrestrial independence of the Isopoda; they are restricted to a fairly narrow niche. Some species have colonized grasslands but in circumstances which are not environmentally very different from leafmold. The most important fact that I wish to convey about the terrestrial Amphipoda, or "land-hoppers" (Bousfield, 1964), is that they exist. Where they are present, they are important both as elements of the fauna and in biomass. In this context, terrestrial is defined as "being independent of the sea or of My thanks are due especially to the patient listening of Dr. J. Laurens Barnard o£ the U. S. National Museum, on whom many of these ideas were tried out; to Mr. J. W. Brodie and Dr. D. J. Cullen of the N. Z. Oceanographic Institute for advice on geological matters; and to Dr. Dorothy Bliss of the American Museum of Natural History for provoking this paper. Mr. J. J. Whalan of the Photographic Section, Information Service, DSIR, produced the black and white photographic illustrations from Kodachromes by the author. I am greatly indebted to Mr. Kelvin Duncan of the Zoology Department, University of Canterbury, Christchurch, New Zealand, who has so generously allowed me to incorporate unpublished information from his continuing work on the ecology and biology of New Zealand terrestrial Amphipoda. Presentation of this paper at the Symposium on Terrestrial Adaptations in Crustacea was made possible by Grant GB-6613 from the National Science Foundation, and by a supplementary travel grant from the New Zealand Department of Scientific and Industrial Research. standing bodies of water for breeding, feeding, and distribution." While there are degrees of acclimatization to the terrestrial environment, most species of terrestrial amphipods are just as independent and just as terrestrial as are woodlice, ants, or myriapods. This amphipod fauna is largely unknown to workers in the Northern Hemisphere because it is absent from Europe, much of Asia and North America, and apparently most of South America, except as accidentallyintroduced and restricted populations, e.g., in California and in various European greenhouses and gardens (Hurley, 1959). As a family, the Talitridae are found on most shores throughout the world, except in the Arctic and the Antarctic. American zoologists may be familiar with the genus Orchestia, which includes many species of common sandhoppers; Smallwood (1905) wrote a notable paper on the ecology of O. palustris ( = O. grillus Bosc, 1802) at Cold Spring Harbor. Sandhoppers belonging to Orchestoidea are common on the American coast (Bousfield, 1957; Bousfield and Klawe, 1963; Bowers, 327 328 DESMOND E. HURLEY 11G. 1. Mtioucyitis pyrijera on a gravel bank near the water's edge—a typical, supralittoral, Urchestia, "rockhopper" New Zealand) 1964). Smallwood (1903) also did pioneering ecological work on Talorchestia, the third of the common genera of "sandhoppers." The terrestrial amphipods ("leaf-mold amphipods" or "landhoppers") are less well known and studied (Hurley, 1959), but sufficient information has accumulated since 1959 to warrant some review. In particular, I should like to acknowledge the work on New Zealand terrestrial amphipods of Mr. Kelvin Duncan of the University of Canterbury, New Zealand, who has very generously allowed me to quote from work in progress. below low-tide. In many ways, it would seem that the greatest problems in the transition from the sea to the land were overcome when the talitrids emerged from the subtidal to the supralittoral. The changes that were necessary are substantial: 1. The surrounding medium is completely changed — substituting air for water requires mechanical as well as physiological adaptation. In an animal like an amphipod, with a particularly unstable body form for terrestrial progression, it could be a major hurdle. Mechanically, it would be much more difficult for an amphipod like Talorchestia to retain its upright attitude than for a stable-bodied animal like the isopod Ligia, with its low center of gravity and even leg spread and length. 2. There is a complete change in primary mode of progression, from swimming to jumping. Although there is, superficially, little obvious morphological difference between Talorchestia and Hyale (one of its nearest marine relatives), there are some important and rather sub- FROM THE SEA TO THE SUPRALITTORAL The supralittoral species, those that live in the zone from low tide to the spray zone above high tide (and sometimes beyond), divide mainly into sand-dwelling or rock-dwelling species. Both are dependent on algal litter (Fig. 1) and other beach debris for food and, to some extent, for shelter. There are no true talitrids (that is, Family Talitridae sensu strictu) habitat. (Island Bay, TRANSITION TO LAND IN AMPHIPODS tie changes. Bulycheva (1957), describes the shortening of the urosome in Talitroidea and the strengthening of pereopods 3-5 and uropods 1-2, necessary for jumping. Her observations on O. gammarella suggest that the animal balances on pereopod 3 while turning the abdomen under the body so that the ends of uropods 3 and the telson press into the sand; pereopods 4 and 5 are parallel to but do not touch the ground. When the abdomen is flexed and straightened out, the animal is propelled into the air. In landing, uropods 1 and 2 and perhaps also pereopods 4 and 5 are used as shock absorbers. Uropods 1 and 2 are strong and spinous; this, she suggests, increases their elasticity, and they act as levers. This state, according to Bulycheva, is anticipated in Hyale, which spends some of its life above water although it is essentially a sub-tidal genus. She notes the shortening of the urosome and the more powerful development of the last 3 pereopods in Hyale, so that, although these legs are not as well developed as in the supralittoral genera, the animal can jump about in search of food or escape by jumping if it is attacked while out of water. Bulycheva stresses the development of a lateral body shield, formed by the sideplates and epimeral plates of the thoracic and abdominal segments, to protect the gills, eggs, and developing young, and perhaps also to preserve moisture in the brood pouch. While the body shield undoubtedly has these protective advantages, one must beware of reading too much into this as a precursor of terrestrial life; many marine genera, especially in such families as the Lysianassidae, Acanthonotozomatidae, Haustoriidae, Stenothoidae, and Amphilochidae, have much better developed lateral shields. 3. Modification is necessary in most of the important functions of life — breeding, breathing, and excreting. Feeding does not require major mechanical adaptation, since the diet involves no more than a progression from under-water 329 algae to above-water algae (wrenched from their under-water context) and then to alternative vegetable matter in the form of decaying leaves, although, as pointed out by Wieser (1967), there are physiological problems, such as a need for copper. The terrestrial species probably evolved from supralittoral species, and were able to enter the leafmold environment directly from the supralittoral zone with little modification and without great difficulty. There is no evidence that they ever passed through a fresh-water or brackish stage. It is as if, having reached the algal debris zone on the beach, they entered a long tunnel that emerged on the land. In the Pacific, the forest frequently goes right to the water's edge, and algae and litter are contiguous. THE CRYPTOZOIC FAUNA The leafmold of tropical and subtropical forests supports a strikingly prolific cryptozoic fauna (Fig. 2). Cryptozoic was first proposed by Dendy (1895, p. 99) for "the assemblage of small terrestrial animals found dwelling in darkness beneath stones, rotten logs, and the bark of trees, and in other situations." He specifically included the amphipods, Orchestia sylvicola from New Zealand, and Talitrus sylvaticus from Australia, amongst the cryptozoic fauna, which consists of "isolated representatives of typically aquatic groups which have as yet become little modified in accordance with their new life... Every naturalist knows how many small animals swarm beneath half-dry stones on the seashore. Such species appear to me to be taking the first step towards a terrestrial life. Gradually, they will make their way inland, still keeping beneath logs and stones for the sake of moisture and coolness, until they finally accustom themselves to a thoroughly terrestrial existence. In this we must place the shrimp-like Amphipoda and Isopoda which certainly look strangely out of place on land." (p. 101) The cryptozoic, or leafmold fauna, is particularly important in Pacific countries, and amphipods are common and numerous. On Stephens Island, 330 DESMOND E. HURLEY 1'IG. 'Z. Cryptozoic animals from a small sample of various insect larvae. The sample is not typileafmold. Included are amphipods, isopods, cal in being remarkably deficient in mites and millipedes, opiliones, pseudoscorpions, beetles, and Collembola. (Khandallah Reserve, New Zealand) Zealand, I have more than half-filled a 2-oz jar with a relatively small amphipod, Orcheslia rubroannualata, from a bag of litter of less than one cubic foot capacity. Similar yields of Talitrus sylvaticus have been taken under hedges of African boxthorn and other introduced plants in Taranaki, New Zealand, while Birch and Clark (1953) have recorded as many as 4000 amphipods per square meter in rain forests near Sydney, Australia. While only 11 species of terrestrial amphipods have so far been recorded from New Zealand, Auckland, and the Campbell Islands, there is little doubt that there are more species undescribed. The other constituents of the litter fauna are also numerous, both in numbers of animals and in numbers of spe- cies. There has been no recent work on isopods, but some 37 species are already known from the New Zealand region. (These are not found in domesticated situations — the introduced Porcellio scaber is the common species found around houses in New Zealand). Casual observation of leafmold samples indicates that many species remain to be described. Lee (1959; 419) lists 36 species of New Zealand earthworms of the Family Megascolecidae found exclusively in leafmold — "they do not make permanent burrows but move about in the leafmold" — and other species found there occasionally, while Forster (1954) has described a number of leafmold Opiliones or "harvestmen" from New Zealand. Other well represented groups include land snails, millipedes, TRANSITION TO LAND IN AMPHIPODS Collembola, mites, weevils, and other arthropods. LEAFMOLD AS A HABITAT The leafmold zone is primarily a humid, insulated, temperate, food-filled habitat. Even a layer only one or two leaves deep, without any great underlayer of leafmold, will keep a drying waterchannel moister than the surrounding non-insulated soil. Within the forest, there is a double insulating effect. The forest canopy insulates against the direct rays of the sun; the leafmold layer is insulated by its surface covering of dry and drying leaves against evaporation within the forest. That terrestrial amphipods introduced to countries where they are not endemic have thrived in greenhouses is no accident, and they have been often listed among the "hothouse fauna" (Kraepelin, 1900). Hatch (1949, p. 162) refers to the isopod, Porcellio dilatatus, as "a propei-ly adapted species which can spread from greenhouse to greenhouse without being able to live in the surrounding situations." Writing of South African forests, where terrestrial amphipods are common, Lawrence (1953, p. 53) made this comparison: "The great surface evaporation of the leaves creates a humid mantle around the forest while the foliage of the canopy blankets the substratum from the direct rays of the sun so that it keeps its moisture longer. The atmosphere... especially upon a hot day, often recalls that of a greenhouse." The leafmold zone is a stable one. Light intensity is considerably reduced by the strata of the canopy above and by the nature of the zone itself. Humidity and temperature are relatively constant. "Forest temperatures are generally lower in summer and higher in winter than temperatures of adjacent areas . . . cooler during the heat of the day and warmer during the night . . . Relative humidity is characteristically higher and evaporation rate lower . . . than in adjacent, less dense terrestrial communities" (Allee, et 331 al, 1949, p. 480). These influences towards a more stable and equable climate are intensified in the leafmold zone with its own built-in insulation. "The cryptozoa are not only sheltered by. .. forest and shrub which mitigate the extremes of light and temperature, but they are further covered by the damp layer of humus which cuts off all light and movements of air, further reducing the comparatively small fluctuations of temperature and humidity that prevail throughout the forest" (Lawrence, 1953, p. 51). Under the leafmold, however, there is a tendency for the sharp boundary between mold and soil to disappear and for decaying leaves, root tangles and friable soil to intergrade so that the ground surface no longer acts as a boundary. In the normal yearly cycle in such situations, there will, nevertheless, be some fluctuations in humidity, rainfall, and free-standing water. Then the annual rhythm, of adaptation to climate is likely to be vertical,1 and not horizontal, although there are reports of migrations by terrestrial amphipods, which are known to travel 30-40 yards in a night (Duncan, personal communication). In the Northern Hemisphere, introduced species have invaded houses and buildings. Ingle (1958) reports Talitrus sylvaticus invading a scullery in Penzance, Cornwall, during a damp summer. Large numbers appeared on the flooded concrete floor, drowned by rain water. Apart from migrations caused by flooding, one may expect a downward retreat to the deeper, moister leafmold layers in drier weather. Unless conditions are abnormal, there is usually sufficient depth of mold to provide a moist reservoir. Observations show that the animals penetrate the friable soil underneath and enter burrows of other animals, although they do not appear to make permanent burrows themselves. In extremely dry conditions i Vertical movement is a characteristic of sawfly larvae in a grassland situation (Waterhouse, 1955). 332 DESMOND E. HURLEY there are usually islands formed by deep pockets in the leafmold, as around rootbases. Fallen and rotten logs also provide refuges. In remnants of native bush, the ecological islands provided by decaying trees and logs on the ground are often the only places where one can find endemic terrestrial isopods, which require much the same environment as terrestrial amphipods. Dendy (1895, p. 119) noted that the cryptozoic fauna generally was far easier to find in partially-cleared localities under fallen logs, than in virgin forest, "where there is so much cover that the animals are widely scattered, and the search becomes very laborious." In Australia, Birch and Clark (1953, p. 18) have noted that in wet years amphipods occur in leaf litter of "drier habitats such as Casuarina, Eucalyptus, and Angophora forests"; in most years the leaf litter in these forests is too dry for Talitrus to survive. However, the fact that repopulation occurs in wet years suggests that some must survive in the "drier habitats" or in close proximity. In this regard, Duncan has evidence that terrestrial amphipods do not occur in New Zealand where the annual rainfall is less than 24 inches. In unusually wet situations, the animals move upwards instead of downwards and may even leave the leafmold entirely. Some years ago, after extensive collecting in Fiordland, New Zealand, where it rains on 195 days a year and the mean annual rainfall is over 250 inches, Dr. R. R. Foster (personal communication) remarked on the absence of terrestrial amphipods in his leaf litter samples. Duncan has since found that saturated ground conditions in Fiordland have driven the amphipods to living in moss and under bark on trees. This may not be unique. On Auckland Island, where the annual rainfall is 82.7 inches but rain has been recorded on 331 days of the year, Mr. J. H. Sorenson collected Orchestia parva "from trunks of rata trees" on Musgrave Peninsula (Hurley, 1957). On the Snares Islands, between Fiord- land and Auckland Islands, terrestrial amphipods can be collected from fern with a sweepnet in wet weather (P. M. Johns, personal communication). In a more normal climate in Canterbury, Duncan has found that, as moisture increases, the animals climb tussock grass. He set out two traps, one sunk in the ground and the other above the ground where it could only catch amphipods falling from the tussock. The heavier it rained, the more amphipods he caught in the upper jar; but in fine weather the upper jar was empty. Thus escape mechanisms are controlled on the one hand by the humidity of the environment and normal reactions to desiccation and on the other by an avoidance of fresh water that does not appear to be unique to the terrestrial species. Smallwood (1905), for instance, has described very similar behavior in the salt-marsh amphipod, Orchestia palustris, at Cold Spring Harbor. CAMOUFLAGE AND ESCAPE BEHAVIOR Under normal conditions reaction to disturbance is simple. The animals are well camouflaged for life in leaf litter, the terrestrial species being a brownish to blackish color, matching the soil and the leafmold they inhabit. When the amphipods are violently disturbed and their cover is removed, they jump very actively for a few seconds, stop momentarily, and then, walking rather than jumping, begin to look for a suitable hiding place. Less violent disturbance tends to release only the walking activity: if there is undergrowth available, the amphipods will disappear into it; if dried leaves, the animals will often disappear into a rolled leaf; if loose soil, they will insinuate themselves into the surface layer (Fig. 3); if leafmold, into crevices in the litter. Duncan has commented that the apparently unsuitable body shape of the amphipod for terrestrial life is actually quite well adaped for life in leafmold since the animal can slip on its side between the 333 TRANSITION TO LAND IN AMPHIPODS FIG. 3. Typical garden habitat after removal of cover (Selaginella kraussiana). Specimen of Talitrus (circle) has completed active jumping phase and worked its way into loose topsoil; it is now playing dead. (Khandallah, New Zealand) horizontal layering without any difficulty. The whole behavior pattern is that of a crevice-seeking animal, not a burrower. To a careful observer, the escape mechanism seems curiously ostrich-like — an animal will place its head into a rolled-leaf and yet most of the body will be clearly obvious. In fact, it is actually well camouflaged; only because the eye has been following an individual specimen does the hiding place seem inadequate. In such crevices, the animal "plays dead." (This reaction can be used when picking up specimens, since both supralittoral and terrestrial species lie quietly if grasped by their sides.) This behavior may be interpreted as having both an active crevice-seeking phase, in which the antennae probably play the greatest part, and a quiescent hiding stage, which is assumed when reaction to pressure on the body, and probably visual reactions to subdued light within a crevice (since often only the head seems to be covered), suggest to the animal that it is adequately hidden. This behavior would seem to be essentially no different from that found in many supralittoral species. SPECIATION Genera Involved. There are at least three distinct lines of development towards the terrestrial habitat. Species of Orchestia (sensu latu), Talitrus (Talitroides), and Talorcheslia are all found in the terrestrial environment.2 The supralittoral species of the Talitridae form a compact group, varying only in combinations of male and female shape and in minor morphological details. Gnathopod combinations are used as the main, somewhat unsatisfactory, generic distinguishing features. There is a tendency for Talorchestia and Orchestia to intergrade in gnathopod shape but this would appear to be due to convergence. There is a fairly clear distinction between Talilnis and Orchestia, suggesting that 2 For a list of species and their distributions see Hurley, 1959; also appendix to this paper which adds later or previously overlooked records. 334 DESMOND E. HURLEV they, at least, have given rise independently to terrestrial species. Origins of Genera The littoral species have a much more cosmopolitan distribution than the terrestrial ones. They also extend a great deal further into the Northern Hemisphere and along the shores of the Atlantic Ocean, being found from Norway (Trondhjemsfjord) to the Falkland Islands with the most species in the Pacific. Bulycheva (1957) compared a Pacific Ocean fauna of 120 species belonging to 12 genera of talitrids (sensu latu) with an Atlantic Ocean fauna of 99 species (9 genera) and an Indian Ocean basin fauna of 27 species (6 genera). She noted that 30 of 34 known species of Orcliestia, 27 of 33 known species of Talorchestia, and 22 of 33 known species of Hyale occurred in the Pacific and suggested that the strong tropical talitrid fauna found in the Mediterranean region was due to past distribution along the southern edges of the prehistoric Tethys Sea, which is said to have linked the Atlantic, Mediterranean, and Pacific Oceans in the Tertiary (Ekman, 1953, pp. 63-64). ized distribution. I believe that this is due to a tendency for supralittoral species to give rise to endemic terrestrial species where there is an available leafmold habitat and access to it from the supralittoral. The morphological differences between supralittoral and terrestrial species are so limited that this explanation seems the most plausible. Otherwise, it becomes difficult to explain the presence of endemic species of terrestrial talitrids on oceanic islands, e.g., Orcheslia kanlensis and O. pickeringi on Hawaii (Barnard, 1955). Tendency to Develop Terrestrial Species It is possible that one or more of the semi-cosmopolitan supralittoral species, e.g., Orcliestia platensis, is able to throw off terrestrial species wherever the situation is appropriate. If this is so, then speciation of leafmold amphipod species may be a secondary stage, the first being an invasion of the leafmold by a supralittoral species. There are indications that this can happen. Chilton (1920) has described a variety of the common Southern Hemisphere rock-hopper, Orchestia chiliensis var. gracilis, from Juan Fernandez Island, 590 meI have previously referred to the terres- ters above the sea shore "under stones." I trial talitrids as an Indo-Pacific fauna have compared his specimens with O. (Hurley, 1959). As more information has chiliensis (sensu strictu) from Juan Fercome to hand, it would seem that the nandez and believe he was correct in givanimals are rather more widely dis- ing them no more than varietal status. tributed through the tropics and the cold- The differences he noted were longer and temperate Southern Hemisphere; never- slender 3rd to 5th legs and antennae; theless, most of the species are of Indo- these are in line with morphological Pacific origin. trends in terrestrial species. It must also be admitted, without In Norway, according to Chevreux necessarily subscribing to any views on its (1900, pp. 2-3), Orchestia littorea (probimportance as a distributional route, that ably gammarellus) are found only at the the southern boundary of the Tethys Sea sea, and along the east coast of France coincides relatively well with the northern "some hundreds of meters from the sea." limit of terrestrial amphipod distribution. In the Balearic Islands, these amphipods There are approximately 50 recorded are found commonly along the edges of terrestrial species of Amphipoda (Hurley freshwater streams many kilometers from 1959; appendix, this paper). Some have a the beach (Chevreux, 1893, p. 125), while fairly extensive distribution (if they have in Algeria, between Biskra and Tougourt, been correctly identified); others — by far numerous specimens have been found in the larger number —have a very local- humid ground at the bottom of a dried- TRANSITION TO LAND IN AMPHIPODS up drain, about 500 km from the sea (Chevreux, 1888, p. 352). Barrois (1888, p. 31) recorded them in the Azores on the cliffs of a peak more than 80 m above sea-level; and de Guerne (1889, p. 357) found they had surmounted an altitude of 410 m and a distance of up to 2 km to reach the water's edge in the interior of the Caldeira de Graciosa. Sachs (1929), as reported by Bulycheva (1957), described "terrestrial" talitrids forming mass aggregations under driftwood on the shore but also moving far inland. Sachs found individual specimens at night in his tent, a considerable distance from the sea. He quotes Dulkeit who noted that "in the fall, in the zone of storms and strong breakers, they move into the taiga and winter under logs, stumps, etc. . . [They] begin to move in the spring, on warmed-up slopes; they follow the receding ice and occupy their summer habitat in the driftwood zone." In the grounds of Leiden Zoological Laboratory, which borders a freshwater canal, Dorsman (1935) found Orchestia bottae common but only where there was suitable vegetation (Petasites hybridus, or reeds, or both). Every year, before hibernation, the amphipods moved away from the canal to higher and drier grounds where they were in no danger from freezing ground water. These reports, and others, indicate that, on occasion, supralittoral species can and do enter terrestrial habitats. 335 reinvasions from the mainland with sufficiently long intervening periods for physiological differences to arise. Similarly, opilionid populations may have been isolated by glaciation and extension of glaciers on the West Coast, South Island. At the other climatic extreme, extensive droughts and bushfires, such as occur in Australia, could cause isolation and initiate speciation. Eruptions, such as the Taupo ash showers in New Zealand which extended over several hundred years and were both intermittent and paroxysmal (Taylor, 1953), could wipe out large sections of invertebrate populations while preserving breeding populations in sheltered valleys and pockets. However, isolating events need not be large-scale. The intersection of meanders in a river is sufficient to form small islands with isolated populations. Rivers and mountain ranges are potential faunal barriers which can isolate leafmold communities. Dell (1955) considers that isolated pockets of scrub would have formed ideal localities in which speciation could have proceeded during glaciation and suggests that the comparatively high number of forms of land molluscs, such as Ptychodon, in Fiordland may reflect isolation of this kind followed by reinvasion. Thus, not only are there possible causative factors, but there is evidence for ecological control of speciation in various groups of leafmold invertebrates. Rates of Speciation Factors Causing Spcciation If one of these supralittoral species penetrates the leafmold and acclimates to living some distance from the sea, one can easily imagine the sudden isolation of a breeding population by any of a number of major or minor accidents. Rise and fall of sea level is an obvious one. Thus, the opilionid fauna of Stewart Island, separated from South Island, New Zealand, by a depth of water of no more than 25 fathoms, is considered by Forster (1954) to indicate a series of invasions and Since the only fossils that are indisputably assigned to the Amphipoda are in Baltic amber and are not talitrids, it is difficult to estimate the antiquity of the terrestrial species. Arguments from geological evidence and paleogeography tend to be circular. However, there are some geologically datable events that may hint at the orders of time involved and at possible rate of speciation. If terrestrial amphipods required a land connection to reach New Zealand, they must have done so in or before the 336 DESMOND E. HURLEY early Cretaceous (Fleming, 1962, p. 105). Even if they arrived then, their distributions, and those of other leafmold elements [earthworms (Lee, 1959); opiliones (Forster, 1954); land snails (Dell, 1955)], show the great influence of subsequent, relatively recent, geological events. Fleming (1962) points out the presence of a rich specialized biota in the New Zealand alpine and montane environment. The topography of this environment is not older than Miocene and its climate is post-Pliocene, and land connections since the alpine biotope arose are out of the question. Reconciliation of its youth with its specialized biota is only possible, according to Fleming, if there was "some rapid evolution and physiological adaptation." I am similarly led to believe that some species, at least, of New Zealand terrestrial amphipods are postMiocene, possibly post-Pliocene. While it is difficult to prove the earliest dates for the origin of terrestrial species, the latest dates for some species can more easily be inferred. Some species of terrestrial amphipods, earthworms, and opiliones are present in New Zealand on both sides of Cook Strait. These species must therefore have originated before the close of the last glaciation (10,000-20,000 years ago), when the sea withdrew 350 feet or more below the present levels to bridge Cook Strait (Fleming, 1962). Other species are established in Stewart Island and the South Island of New Zealand. Here, where a fall in sea level of only 15-20 fathoms would establish a land connection, there is evidence of an old shoreline at 35 fathoms, 11,000 years ago, and a rapid rise in sea level between 11,000 and 9,000 years ago which inundated the area (Cullen, 1967). Morphological Changes The type of morphological change associated with speciation is fairly simple. I have suggested (Hurley, 1959) that some species have arisen through the retention of juvenile or embryonic characters in the adult. This is suggested especially by the gnathopods. Gnathopods. In many species of Orchestia, including all the supralittoral ones, the second gnathopod in the male is a large subchelate "grasping hand." This type of gnathopod is used in littoral talitrids to carry the female during copulation. However, in Talitrus, the male second gnathopod is small and feebly chelate, and in the females of both genera the hand is small and feebly chelate, superficially indistinguishable from that of the male Talitrus. Terrestrial species of Orchestia show gradations in size and type of male second gnathopod from the typical large supralittoral form to one not unlike the typical Talitrus form. The intermediate forms are strikingly like stages in the development of the male second gnathopod in supralittoral species (Figs. 4 and 5). The possibility that these are subadult forms is generally contradicted by other evidence from morphology and distribution. Pleopods. A striking feature of terrestrial species is a trend towards loss of pleopods. In the marine and supralittoral species, there are normally three pairs of well-developed, well-segmented, setose, biramous pleopods. At the other extreme, the terrestrial species, Orchestia patersoni, has three pairs of vestigial triangular stumps. This loss would not appear to be neotenous; there are no records of juvenile post-embryos with vestigial stumps that later develop into recognizable pleopods. However, reduction of pleopods does seem to occur in step with reduction of gnathopods (Fig. 5). It seems likely that the variation in pleopods is associated with environmental and breathing requirements. In marine species, pleopods are used for swimming, drawing water over the gills, and directing food currents past the gnathopods. While the change to a surrounding air medium might have been expected to render pleopods useless, some terrestrial species still have fully de- TRANSITION TO LAND IN AMPHIPODS 337 FIG. 4. Talorchestia bottae. Three successive stages in development of second gnathopod of male. (After Chilton, 1921; from Hurley, 1959) veloped pleopods, suggesting that the pleopods are still functional, and pleopods are present in all supralittoral species. One possible function is to create air currents past the gills. Duncan found that terrestrial amphipods retain some water ("exosomatic water") in their brood pouches, and suggested that the pleopods may prevent its stagnating. Some terrestrial amphipods will die in a matter of hours when accidentally immersed in water, and pleopods might assist them to escape. However, some species do not attempt to swim under these conditions. The South African Talitrus eastwoodae, which has biramous pleopods, "never swims when placed in water and is evidently unable to raise itself above the bottom of a glass jar, moving around in it precisely the same way as if walking on dry land" (Lawrence, 1953, p. 87). Terrestrial species may lack one, two, or three pairs of pleopods, not necessarily in a constant progression from front to rear or vice versa, and the loss is not obviously correlated with altitude or distance from the sea. Orchestia sinbadensis, for instance, has fully developed pleopods although it has been collected 2,0003,000 feet above sea level. It does, however, come from a notably wet area (Milford Sound, New Zealand), and the male has an extremely large second gnathopod. It has been suggested that pleopods could be used to circulate air in burrows, but the terrestrial species do not appear to be active burrowers, although they are crevice seekers and occasionally occupy the burrows of other animals. It may be that agitation and possibly oxygenation of exosomatic water is the most important function of pleopods in those terrestrial species which still have them since Orchestia patersoni, which has no pleopods, has very little exosomatic water. The absence of pleopods in O. patersoni is the logical end-product of the change of medium. Development of Gills. There is a considerable development of gill surfaces in 338 DESMOND E. HURLEY Orchestra leslrensn V V Orchestro rubroonnulata V V Orchestra sinboden! V Orchestra paterjonr FIG. 5. Adult male second gnathopods of five species of New Zealand terrestrial amphipods showing similarities to juvenile and developmental stages of other species of Talitridae (Fig. 4). Diagrammatic representations of the pleopods are given for each species. (The number of segments for each ramus corresponds to the number suggested by setation; in some species, actual segmentation appears superficial or incomplete.) (From Hurley, 1959) most terrestrial species. In Talitrus sylvaticus the gills of both 2nd and 4th legs are very greatly expanded. Bulycheva (1957) contrasts the smooth gills of marine species with a wrinkling or folding of the gills in "terrestrial" species that increases the surface area of the gills while maintaining or even permitting decrease of their overall size. Neither Duncan nor I have observed this. Certainly, there is nothing like the accordion-like pleating of the gills which is found in some genera of the marine family, Lysianassidae, e.g., Ichnopus. Bulycheva also mentions unicellular skin glands in the integument of body somites and appendages. These are said to secrete a fluid that prevents the body from drying in air and "sometimes encompasses the entire body." She presents no documentation of this and it is something neither Duncan nor I have observed. The gills are not particularly protected in the terrestrial species; if anything, their greater size makes them more vulnerable than in marine species. General Morphology. In terrestrial species there is a trend away from the thick, heavily-spinous appendages of the supralittoral species to slender, finely-spined legs, antennae, and mouthparts. The heavy spines of the supralittoral species are often replaced by fine tactile setae. There are, however, no signs of the antennal calceoli common in many marine species of amphipods. Exoskeleton. The smooth, relatively fragile exoskeleton of the terrestrial amphipods contrasts strikingly with the heavily chitinized exoskeleton, often ornamented with knobs and processes, frequently found in terrestrial isopods. The development of this heavy armor, along with the development of pseudotracheae, and the ability to roll into a ball, has probably enabled isopods to enter more stringent terrestrial environments than the amphipods. Nevertheless, the most common leafmold isopods, the Trichoniscidae, tend to have a thin, relatively unornamented, almost transparent exoskeleton, like the amphipods (Fig. 2). Uropods. In some terrestrial species, there is a strong "inter-ramal spine" alongside the rami of the first uropod. Duncan has found that this is used in molting which is very rapid, Orchestia tenuis taking about an hour to cast off its exuvia. The inter-ramal spine is used to help remove the exuvia of the second antennae when these are passed between the rami during the later stages of molting. "The exuvia are neatly flicked off when the abdomen is TRANSITION TO LAND IN AMPHIPODS flexed." Duncan suggests a possible connection between presence or absence of this spur and longer or shorter second antennae. Mouthparts. Here there is a tendency toward strength and simplification. The strongly dactylar 4th segment of the maxilliped found in littoral genera, such as Hyale, is replaced by a shortened, rounded, terminally spinose, almost vestigial segment, sometimes apparently fused with the 3rd. Other differences include the reduction of maxilla 1 palp to a vestigial stump in the terrestrial species. Pellucid Lobes. These are semi-transparent, non-musculated, highly-vascularized lobes with a scabrous surface, apparently without nerve connections, found especially on the second gnathopod of the female. Since the males of the same species do not have them, it is unlikely that the lobes are necessary for feeding; rather, reduction in size of the large second gnathopods and simultaneous development of these processes in terrestrial species indicate changes in sexual habits. Mclntyre (1954), has described how the peculiarly-twisted, second gnathopod, which is well supplied with these processes, is used by the female to comb the broodplates. Duncan has seen ovigerous females using these gnathopods to turn the eggs. (It has been facetiously suggested that the cave-man tactics of supralittoral and marine males in grabbing and carrying females have given way to a more seductive approach, and the male processes are used to stroke the female into submission.) In terrestrial species, Duncan has observed male and female lying quietly together without holding, although the antennae are used to retain contact. Undoubtedly, there are behavioral changes here related to changes in fertilization. FERTILIZATION In aquatic talitrids, it is common for the male to carry the female for several days before she molts; then copulation occurs immediately after molting. There 339 is no carrying in supralittoral species of Talitrus (Williamson, 1951). The male of Talitrus saltator does not have a large second gnathopod and, instead, holds the female with its stout second antennae and its pereopods. In this species, the sperm are relatively inactive and large — about 400 microns long. They can live at least four days in the brood pouch, so copulation can take place any time between molting and egg-laying, which occurs four days after molting. Williamson assumes that the sperm are probably activated either by a secretion of the unfertilized egg or by a secretion released by the female during laying. He suggests that these factors increase the possibility of fertilization, since delayed egg-laying allows a longer period during which fertilization can take place, and the male does not have to hold the female until fertilization — a chance meeting may suffice. There is a great reduction in the number of eggs produced in the supralittoral and terrestrial species, compared with the marine ones. In the littoral Allorchestes novizealandiae, a female taken at random had 161 eggs; in most species of terrestrial amphipods examined, the number varies between 1 and 10. In Talitrus sylvaticus, the average is between 3 and 4. Duncan believes that female talitrids lay sufficient eggs to fill the brood pouch but that, as the eggs grow, the pouch becomes overfull and some are lost. This can easily happen accidentally, particularly when the female turns the eggs, as the brood plates are not close together. A similar trend was noted by Bulycheva (1957, her table 1) who found that most species of supralittoral talitrids carried 10 to 20 eggs while littoral and marine Talitroidea, Gammaridea, and Amphithoidae had 50 or more — Amp hit hoe tarasovi up to 226. She concluded that terrestrial talitrids had developed larger eggs with a greater reserve of nutrients. Sexton (1924) showed a similar decrease in numbers of eggs from marine to littoral species of Gammarus, but the fre- 340 DESMOND E. HURLEY quency of breeding was greater than in talitrids. The marine G. locusta had up to 143 eggs; the brackish G. chevreuxi, 30-40; the freshwater G. pulex, 12-8, and a littoral species of Gammarus, also 12-8. The terrestrial Talitrus eastwoodae produces 6-14 eggs. However, T. eastwoodae has only one annual brood (Lawrence, 1953), whereas G. pulex breeds five times a year (Hynes, 1955), and in G. chevreuxi, with a breeding lifetime of only 12-18 months, one female produced 29 broods (Sexton, 1928). The incubation period in New Zealand terrestrial species is about two weeks in summer, longer in winter-acclimated specimens (Duncan). Orchestia bottae in Holland has a similar incubation period (Dorsman, 1935). Thus, eggs are larger and fewer in terrestrial than in marine species, but the young emerge larger and more fully developed. MOISTURE REQUIREMENTS The terrestrial amphipods have solved the most important problem, of moisture by remaining in a habitat where humidity is high. Amphipods are very susceptible to desiccation, much more so than the thicker-bodied isopods, although the bodies of the leafmold Trichoniscidae are also thinly chitinized. Edney (19516, 1954) noted that the terrestrial species of isopods have not developed the waxes found in insect cuticles which, he says, have contributed largely to the success of the insects as terrestrial animals. There are other ways of conserving water available to terrestrial species. The ability to evaporate water rapidly, and thus cool the body, found in terrestrial isopods, may help the survival of animals exposed to high temperatures for short periods (Edney, 1951a). This possibility is supported by measurements of transpiration, which suggest that high rates of transpiration are a feature of cryptozoic arthropods (Edney, 1954). My own casual observations suggest that the exoskeleton of terrestrial amphipods is highly permeable and that, by inference, rates of transpiration may also be high. Certainly, death due to desiccation is particularly rapid. Humidity-Tolerance In two species of intertidal amphipods at Woods Hole, Talorchestia megalopthalma and Orchestia agilis, Platzman (I960) a difference in humidityfound tolerance. At 0% R.H. and 26.5°C-the Talorchestia survived for an average of 44 minutes and Orchestia for 33. (This compared with 13.5 min. for a marine amphipod, Amphithoe sp., and 429 min. for a terrestrial isopod, Armadillidium vulgare.) However, there was not sufficient difference in humidity-tolerance to restrict the intertidal amphipods to different intertidal habitats, Orchestia being found under moist seaweed at high tide level; Talorchestia in 1 to 5 inches of sand with a lower distribution 3-4 feet above the watermark at all tidal phases. Orchestia was active night and day, Talorchestia generally only on the surface of the sand near the water at night. Platzman concluded that behavioral and distributional differences in these two species were more important than relative humidity in differentiating their niches. Emergence from Leafmold While it is true that the nature of the forest community makes it unnecessary for many plants and animals to have the specific adaptations to conserve water that would be essential in other terrestrial environments (Allee, et al., 1949), some species of amphipods are able to venture forth from the true leafmold environment. I have seen Talitrus sylvaticus several hundred feet above sea level in Brooklyn, (Wellington, New Zealand), under dry rock and grass debris on a concrete path, or cohabiting with Porcellio scaber under rocks on dry ground where only the slightest moisture was apparent (Figs. 6 and 7). TRANSITION TO L A N D IN A M PHI PODS 341 FIG. 6. An early summer grassland habitat. Talitrus sylvaticus was found under the stones. It would also be present in the rank grass. (Brooklyn, New Zealand) Talitrus sylvaticus seems to have considerable ability to survive outside true leafmold. In Wellington, it is present almost everywhere in gardens. It is possible to find it in any vegetation providing a minimum of cover —under "moss" (Selaginella kraussiana), under Tradescantia fluminensis ("wandering Willy" or "wandering Jew"), wherever there is sufficient cover to provide a run (Fig. 8). In fact, a pile of freshly-cut grass and weeds left overnight on a bitumen path in summer is enough to attract a population of sylvaticus colonizers. In Canterbury, New Zealand, two species of Orchestia occur in tussock grassland (Duncan). In many ways, this grassland is an extension of the leafmold habitat; there is a debris-layer of rotting grass and roots just above the ground and, according to Duncan, the various L, F, and H layers can be recognized. Waterhouse (1955) found that such a matted basal layer of dead grass in wild grassland was important in maintaining a cool, hu- mid atmosphere next to the ground and it completely sheltered insects that were sensitive to radiation. The relative humidity in this layer is close to saturation (above 90% R.H. "at lower levels in the 'mat' of dead grass and stalks," p. 67) and the air is calm, so that small invertebrates are protected from desiccation by the wind. Differences in Grasslands Duncan makes the point that water relations are much more variable in long grass than in leafmold. An undescribed grasslands species of Orchestia that he has been studying can make a temporary burrow in the soil during drought but in flooding conditions climbs up the vegetation "and so avoids osmotic stress." Two typically leafmold species, Orchestia patersoni and O. tenuis, which often invade long grass, cannot do this, and are retricted to more favorable areas in grassland, such as under the canopy of cocksfoot grass. 342 DESMOND E. HURLEY FIG. 7. Undersurface of rock shown in Figure 6. Note Porcellio scaber (several specimens) on rock, relative dryness o£ ground. (Brooklyn, New Zealand) FIG. 8. Typical garden situation in which terrestrial amphipods may be found. The weed is Oxalis sp. (Khandallah, New Zealand) Orchestia patersoni normally lives in podocarp forests, where its biomass is directly related to the thickness of litter in relatively constant soil conditions (Duncan), and occasionally in grasslands under grass canopies. Where it is the dominant species, it does not carry sufficient exosomatic water to enable accurate measurements of its volume, indicating, no doubt, sufficient humidity in the environment. This may explain its lack of pleopods. In subdominant situations, it carries a highly variable amount of water. The new grasslands species of Orchestia lives in grass litter layers down to sea level, but it may be found under high snow tussock up to 3,500 feet. There, it lives under stones and sticks, and in the burrows of native worms and other animals. It carries considerably more exosomatic water than O. patersoni. (The osmotic concentration of this water is about 30% that of seawater. Its volume in most species depends on the size of the animal and varies in weight from 30% of total body weight in the smallest animals to 10% in the largest, the actual amount being apparently regulated by the animal itself.) Duncan also points out (personal communication) that temperature extremes are greater in grass than in forest, so that the ability to acclimate to temperature in winter would be an advantage to a nocturnal surface feeder. The new grasslands species of Orchestia and Talitrus sylvaticus can both do this. Tolerance to Immersion and Need for Water Dorsman (1935) kept Orchestia bottae alive "for many months" in an aquarium filled with water where they could not leave the water. Bulycheva (1957) found a more positive dislike of water. Speaking apparently, of Orchestia gammarella TRANSITION TO LAND IN AMPHIPODS and O. montagui, she said it was "atypical" of them to stay in water and, if they were prevented from leaving, they died within a day or two. "When the orchestiids get into water, they swim vigorously at first, but then make for the bank and jump ashore." Mokievsky (1949) observed similar behavior in talorchestiids. Duncan found that the leafmold species, Orchestia patersoni, which has a very small gill area, died in freshwater in about 2 hr. Death appeared due to a very rapid incursion of water into the gills, causing their distention. His new. grasslands species of Orchestia lasted longer, and distention of the gills was not so rapid, but death was still relatively quick. It is clear from observations of leafmold species in New Zealand that they do not need standing water at any time in their life cycle for breeding or for general well-being. The relatively high humidity of their normal environment reduces evaporation to a minimum, and whatever liquid water is required can be obtained from dew and from rainwater. Their behavior patterns are oriented towards retaining water by remaining in a suitably humid environment, but it is also obvious from the grasslands occurrences that a considerable penetration of apparently non-humid environments has been made by some species. EXCRETION There has been little work on excretion in terrestrial amphipods. Dresel and Moyle (1950) studied excretion in various amphipods and isopods, including a supralittoral Orchestia, and concluded that more than half of the total soluble non-protein nitrogen of the excreta was disposed of as ammonia, the level of nitrogen excretion being lowest in the terrestrial species. They believed this indicated that the animals adapted to terrestrial conditions by suppressing nitrogen metabolism rather than by transforming nitrogenous wastes to other, less toxic products. In terrestrial isopods, they 343 found that 5-10% of the total soluble non-protein nitrogen was present as uric acid and suggested that these minor excretory components might be derived from purines following the loss of one or more of the uricolytic enzymes. They also found a positive correlation between the uric acid content of the tissues and the degree of adaptation to terrestrial conditions; this they attributed to a reduced rate of excretion in the more xerophilous species, rather than to a fundamental difference in metabolism. COPPER REQUIREMENTS Wieser (1967) has pointed out the importance of copper for Malacostraca; whereas marine species of isopods can extract it from seawater, terrestrial species must find another source, probably from food. Experiments with the terrestrial Porcellio scaber and the intertidal Ligia oceanica and Orchestia gammarella indicate that they can extract copper from their food only when the copper is present in very high concentrations. Wieser suggests that, in nature, copper would have to be liberated from plant material, probably by micro-organisms; that the ability to extract it varies with different species (terrestrial species can extract up to 95% of the copper present in artificially enriched leaf litter and seaweed, whereas intertidal species can manage only about 50% at most, usually about 20%), and that more copper is stored in the hepatopancreas in the terrestrial species and it is more strictly tied up. Extensive movements of copper in Porcellio scaber, for instance, require the synthesis of special "carrier proteins," whereas in the marine and intertidal species the copper is able to move more freely in an easily dissociable state between the storage cells and other cells of the hepatopancreas. Since terrestrial isopods stockpile far more copper than is necessary, Wieser suggests that they may "have had to reinvent this old principle of chelation and 344 DESMOND E. HURLEY transport of heavy metals by proteins... to guide their stockpiles safely through the maze of metabolic processes going on in the same organ in which the metal has to be stored." OXYGEN CONSUMPTION In Talitrus sylvaticus, Clark (1955) found that the respiratory rate of small animals (mean body weight 1.5 mg) increased more rapidly above 15°C than in medium and large animals. This is normal for Crustacea, but he also found seasonal differences in oxygen uptake. Oxygen consumption of T. sylvaticus in winter was approximately 1.5 times that in animals of the same body weight in summer, and winter consumption corresponded to that at a temperature 2.5 °C higher in summer. Thus, these amphipods were not able to adjust their rate of oxygen uptake sufficiently to maintain the same rate of energy output in winter as in summer. By covering the gills of terrestrial amphipods with paraffin wax, Duncan did not deprive them of sufficient respiratory activity to cause death, but he believes that normally up to 60% of respiration takes place through the gills. ZOOGEOGRAPHY I have previously asserted (Hurley, 1959) that terrestrial amphipods are confined to countries bordering the IndoPacific, with the exception of South America from which they have not been recorded. European and North American records can be traced to accidental introductions. Since then, terrestrial amphipods, all believed to be endemic, have been reported from Jamaica, Haiti, Panama (Barro Colorado), and Western Australia. More important, I have previously overlooked a number of well-founded references in the older literature to terrestrial occurrences in the Canary Islands, the Azores, Algeria, Tunisia, Cyprus, and West Africa. These records indicate that the distribution of terrestrial amphipods is wider than originally supposed, and that they must be considered to have a tropical and Southern Hemisphere distribution (Fig. 9). They are present on some subantarctic islands, but absent from Antarctica. In the Northern Hemisphere, they are found in Japan, the Philippines, and the Indo-Malayan region. Explanations for Present Day Distribution 1. Continental Drift. This tempting explanation for the present-day distribution of terrestrial amphipods is not without its problems. For some invertebrates, it seems necessary to postulate a Gondwanaland connection in the past to explain occurrences in widely separated southern continents. For example, midges belonging to the blepharocerid genus, Edwardsina, are found only in Tasmania, the high alpine country of Eastern Australia, and cold temperate South America. The genus is archaic and at least of Mesozoic age, and the adult flies remain throughout their life near cascades. Because of this restricted habitat, and because all blepharocerids in the Northern Hemisphere belong to different genera, it seems likely that the distribution of Edwardsina dates back to a period when Tasmania, Australia, and South America were much closer together than they are today (Evans, 1958). Evans believes that this distribution, and those of other plants and animals, suggest that, up to the middle or late Mesozoic, Tasmania, South America, New Zealand, Australia, South Africa, and Madagascar have either been in direct contact with each other or have been, with Antarctica, part of a larger continental landmass. If Evans is correct (and many contemporary geologists are strong proponents of the theory of Continental Drift), such a situation would explain much of the present distribution of terrestrial amphipods. If terrestrial amphipods are really absent from South America, one could infer 73 r c X o o FIG. 9. World distribution o£ terrestrial Talitridae (excluding European greenhouse records). 346 DESMOND E. HURLEY that the group originated in the interval between the separation o£ South America from Africa, and of Jndia from Madagascar and South Africa. This would take us back to the early Tertiary at least (Harrington, 1962; Darlington, 1965). I favor a much more recent origin. Certainly, another explanation must be found for the occurrence of species on oceanic islands, such as Hawaii, which originated much more recently. 2. Distribution along Continental Margins and Island Arcs. The essential element in such a land-bridge hypothesis would seem to be continuity of suitable habitat along dispersal routes. A Pacific dispersal centered along the eastern coast of Asia that extended as far north as present-day Japan, south to India, down the Malaysian archipelago to Australia, New Caledonia, and New Zealand, and through the Pacific Island chains is appealing. This implies an eastward migration through the Central Pacific.3 the route being perhaps provided by Menard's postulated Darwin Rise and, to a lesser extent, his Melanesian Rise. The Darwin Rise is visualized as extending from the Tuamotu Islands to the Marshall Islands about 100 million years ago in a uniquely volcanic region where hundreds of volcanoes developed. "Where they were close together they ponded lava flows and built up enormous ridges. . . For some time the Darwin Rise was dotted with volcanic islands but eventually most of them became extinct and were cut to platforms just below sea level" (Menard, 1964, p. 138). If a Darwin Rise route were open, it might provide an explanation of the Central American and Caribbean distribution. The Early Tertiary would appear to be the latest possible period that terrestrial amphipods could have reached New Zealand by an island-arc land connection (Fleming, 1962; Darlington, 1965). After 3 For other examples of similar distribution patterns see Xakata (1961) and Quate (1961). this time, transport across sea would have been necessary. The difficulty with this land-bridge hypothesis is the lack of explanation for the African distributions. The southern African distribution could be explained by a continuous ecological environment in the past between the areas of present-day southern and eastern Africa and India. Terrestrial amphipods have not yet been recorded in East Africa north of Zululand, but there is reason to believe that investigations of rain forests farther north would provide more northern records. There are podocarp forests from Lake Victoria almost to the Red Sea up the Great Rift Valley (Florin, 1963), and if the Red Sea and the Gulf of Aden are of relatively recent geological origin, little past climatic change may have been needed to provide a continuity of ecological climate along the coastline to India. Admittedly, this is a very simplistic approach, but complete continuity of land is probably not needed. The North African distribution (Tunisia, Algeria, Canary Islands, Azores, Annobon Island) is harder to explain, but the answer might again be found in past climatic regimes and past continuity of environment. The continental margin — island arc explanation depends upon the existence in the past or present of corridors of continuously suitable environment. A by-pass of this nature has been noted along the eastern edge of Australia "open to some plants and animals that cannot tolerate acute aridity. The platypus . . . occurs along this corridor from tropical Queensland to south temperate Tasmania. Flightless forest-living Carabidae, too, extend along this corridor from north to south, the tropical and south-temperate groups meeting and overlapping complexly" (Darlington, 1965, p. 45). 3. Local Origins from Littoral Species. Both of the above explanations in their simplest form are based upon a single origin of the terrestrial Talitridae. How- TRANSITION TO LAND IN AMPHIPODS ever, I believe that these talitrids have arisen independently more than once. The wide distribution of a parent stock is no great problem. In the Southern Hemisphere, rafting of vegetation and algae in the West Wind Drift provides one obvious dispersal mechanism. Wood from South America has, for instance, been collected on Macquarie Island and Tasmania (Barber, Dadswell, and Ingle, 1959). Bolin (1967; personal communication) reported live ants on a floating bamboo island in the Bismarck Sea, out of sight of land (03°45' S, 149°45'E). Stock and Bloklander (1952) recorded 26 species of amphipods found on floating objects washed ashore on the Dutch Coast. Although none of the amphipods were talitrids, and some of the objects may have originated on the Dutch Coast in the first place, these records indicate the possibility of the transport of a littoral or supralittoral parent stock. The occurrence on Solander Island, New Zealand, of the terrestrial amphipod, Orcheslia patersoni, suggests transport by rafting. Solander Island is of volcanic origin, and the exposed rocks are probably of Upper Pleistocene age, perhaps of the last glaciation (Harrington and Wood, 1958). It stands in water too deep to have been open to colonization across land due to falls in sea level. The species concerned has also been recorded from Snares Island (about 90 miles away), Stewart Island (40 miles), and South Island, not quite 25 miles away. Introduction could, less possibly, be due to man, improbably to transport on birds. While transport by sea birds, especially burrowing sea birds, is possible, since terrestrial amphipods are likely to be caught up in feathers during nest scuffling, resistance to desiccation from either wind turbulence or the heat of the bird's body presents considerable problems. 4. Distribution by Man. In recent times, man has been responsible for distribution of terrestrial amphipods; this has been shown by occurrences in the tropical pits at Kew and in California. 347 How often this has happened in both the historical and prehistorical past is problematical, but examination of the affinities of widely spread species may clarify this. I believe that the very widespread distribution of some species in the Pacific (Fig. 10) must be partly due to man4 — and certainly illustrates the possibility of wide dispersion, without obvious recent geological connection. There has been ample opportunity for some dispersal by man. Taros and yam plants in Polynesian and Melanesian canoes; coffee to Indonesia; frangipani from Ceylon to the Cook Islands; cocoa and breadfruit to the Caribbean; ancient horticultural ventures in the African and Mediterranean regions — these are but a few of the possible horticultural crosscurrents of transport. Of the four suggested possibilities, I believe that the last three have played the major but varying part in the distribution of terrestrial amphipods. Probably the most important has been the existence in the past, but not necessarily at one time, of a continuity of suitable environment provided by climate, vegetation, and land connections particularly in the IndoPacific region. There is a remarkable coincidence of the distribution of terrestrial amphipods as presently reported (Fig. 9) and the distribution as given by Florin (1963) of the podocarp forests of the world (Fig. 11). Climate has probably been more important than land connections in the distribution of conifers and taxads (Darlington, 1965, p. 191). "Their distribution can probably be reconciled with any reasonable history of the world: stability of continents, or continental drift, or antarctic land bridges. [It] seems consistent with any of these hypotheses, and proof of none." The distribution of podocarps and terrestrial amphipods may not have followed the same route, but the coinci* Dahl (1967) reports that Talitrus pacificus and T. alluaudi appear to have been introduced recently to the Azores, where T. pacificus may be replacing the endemic Orcheslia chevreuxi. 348 " ^ DESMOND E. HURLEY TERRESTRIAL TALITRIDAE [FT] Talorchestia diemensis Q Orchestia anomala 0 Talitrus alluaudi r ? [31 Talitrus s/lvaticus (J [x] Talitrus pacificus FIG. 10. Reported distribution of some terrestrial Talitridae in the Pacific. dence of habitat and inhabitant deserves investigation. Although overall possibly less important, independent entry of supralittoral species into the leafmold environment in different land masses and particularly on individual islands is likely to have given rise to some of the endemic species. Finally, the picture has been confused by distribution by man or by accident. Anomalies in Distribution Absence from South America. The absence of records of terrestrial amphipods from South America is mystifying since there would seem to have been ample opportunity for endemic species to have arisen from local supralittoral ones and every likelihood of it happening. The Central American and Caribbean records make the absence of reports from South America even more surprising, especially since Bousfield (1964) has reported a littoral Parorchestia from Uruguay. At my request, Professor G. A. Knox searched for terrestrial amphipods during the Royal Society's Chilean Expedition and found none. It may be that in South America, as in the Campbell Islands, they will be found in unusual habitats, such as in the moss on trees or under the bark of trees. Absence from the Northern Hemisphere. The northernmost records of truly terrestrial species are from the Mediterranean in Europe and Japan in the Eastern Pacific. It is probably coincidence that the northern limits in the EuropeanMediterranean region approximate the suggested southern shores of the Tethys Sea; other reasons should be sought for their absence from Northern Europe, Asia, and America. Apart from Orchestia and Talorchestia, the commonest supralittoral amphipods in North America belong to Orchesloidea, which does not seem to have given rise to terrestrial species. Ice-shields in the Northern Hemisphere may have been a barrier in the past. Absence is not due simply to the difference in plant cover, *>•/ 60" t o 2 "8 K •5 o 3 180* 160* 140* 110* 100- 80" 60* 40* 20- <T 20" 40" «>• 100" 120* 140* 160" 180" Podocarpus: total present distribution — C D ; distribution in the past — ?early Jurassic^, middle Jurassic • , Hate Jurassic^. ?early Cretaceous B. late Cretaceous • , Eocene ffi. Oligocene (in New Zealand incl. Oligo-Miocene) C, Miocene © , Pliocene • , Tertiary (indeterm.) ® . FIG. 11. World distribution of the genus Podocarpas. (After Florin, 1963) 350 DESMOND E. HURLEY since introduced terrestrial species have ment, although some species have emerged acclimatized themselves to restricted habi- into grassland conditions; the major phystats in the Northern Hemisphere, and ter- iological adaptations were already made restrial amphipods can be found in exotic when the species which colonized the supraNorthern Hemisphere plant associations littoral zone emerged from the littoral; terin New Zealand, such as the large, man- restrial species are of southern and tropical distribution, and where they exist they are made Pinus radiata forests. Absence is not due to leaf-fall alone; important members of the leafmold fauna endemic species are common in New both in numbers of species and biomass; Zealand beach forests. Winter climate and their distribution may be in part due to disground freezing may have some effect, persal along suitable environmental corriand the success of introduced elements dors around the eastern Indo-Pacific, in part may be due to man-made changes in envi- by local speciation from supralittoral speronment opening up otherwise arid or cies, and in part by human introduction; unsuitable climates. I am told that tali- and, finally, they present a fascinating optrids in California are now infiltrating the portunity for further physiological and Imperial Valley in the wake of irrigation distributional investigations. (Dr. J. L. Barnard, personal communication). APPENDIX Darlington (1965, p. 131) makes the A. New species of terrestrial Amphipopoint that northern continental climates da subsequent to or omitted from Hurley are unique; plant and animal distribu(1959:109). tions reflect the fact that the oceanic cli1. Talitrus (Talitropsis) fernandoi De mates of smaller southern land-masses are Sylva. Ceylon (De Sylva, 1959) in some ways more like tropical than 2. Talitrus nesius J. L. Barnard. Caronorth-temperate climates. Tree ferns, line Islands: Ponape (J. L. Barnard, conifers, and Peripatus, for instance, are 1960) almost world-wide in suitable tropical 3. Talitrus toli J. L. Barnard. Caroline and south-temperate zones but do not exIslands: Truk (J. L. Barnard, 1960) tend into the north-temperate zone ex4. Talitrus trukana J. L. Barnard. Carcept very slightly into southeastern Asia. oline Islands: Truk (J. L. Barnard, Consequently, he suggests, southern cold1960) temperate plants and animals can dis5. Orchestia canariensis Dahl. Canary perse through tropical and sub-tropical Islands (Dahl, 1950; Andersson, areas more easily than north-temperate 1962) plants and animals. 6. Orchestia chevreuxi de Guerne. A difference in climatic environments Canary Islands, Azores (de Guerne, between hemispheres seems the most like1887, 1888a, 1888b; Chevreux, 1900; ly reason for the absence of endemic terDahl, 1950, 1967; Andersson, 1962) restrial amphipods from Europe and 7. Orchestia ponapensis Barnard. CaroNorth America. line Islands: Ponape (Barnard, 1960) SUMMARY 8. Parorchestia1 campbelliana Bousfield. Bousfield regards Parorchestia as a In conclusion, terrestrial amphipods valid genus, not as a subgenus of Orexist; they will drown in water; they have chestia. Campbell Island (Bousfield, conquered the land more by behavioral 1964) than morphological adaptations — if, by B. Additional localities for terrestrial conquering the land we refer to their leaving the seashore for inland forests; species listed in Hurley (1959:109). these behavior patterns have tended to 2. Talitrus alluaudi. Madagascar (K. restrict them to the leafmold environ- H. Barnard, 1958). Canary Islands (An- TRANSITION TO LAND IN AMPHIPODS dersson, 1962). Finland, (Palmen, 1949). Azores (Dahl, 1967) 5. Talitrus hortidanus. Caroline Islands: Palau, Truk (J. L. Barnard, 1960) 7. Talitrus pacificus.2 Reunion, Comores, Madagascar (Ruffo, 1958; Paulian, 1961). Azores, Madeira (Dahl, 1967). 8. Talitrus sylvaticus. Cornwall (Ingle, 1958); San Francisco (Bousfield and Carl ton, 1967) 10. Talitrus topitotum.2 Madagascar (K. H. Barnard, 1958); California: Pasadena, Balboa Park (Bousfield and Carlton, 1967) 18. Orchestia floresiana. Caroline Islands: Palau, Yap, Sonsorol, Kapingamarangi, Kusaie. Gilbert Islands: Onotoa. Fiji: Vitilevu (Barnard, 1960) Orchestia floresiana vitilevana Barnard 1960. Fiji: Vitilevu (Barnard, 1960) 22. Orchestia insularis. Campbell Island: many additional records. (Bousfield, 1964, as Parorchestia (?) insularis) REFERENCES AJlee, W. C, A. E. Emerson, O. Park, T. Park, and K. P. Schmidt. 1949. Principles of animal ecology. W. B. Saunders Co., Philadelphia. 837 p. Andersson, A. 1962. On a collection of Amphipoda of the family Talitridae from the Canary Islands. Ark. Zool. n.s. 15:211-218. Barber, H. N., H. E. Dadswell, and H. D. Ingle. 1959. Transport of driftwood from South America to Tasmania and Macquarie Island. Nature 184:203-204. Barnard, J. L. 1955. Gammaridean Amphipoda (Crustacea) in the collections of the Bishop Museum. Bull. Bernice P. Bishop Mus. 215:1-46. Barnard, J. L. 1960. Insects of Micronesia. Crustacea: Amphipoda (Strand and terrestrial Talitridae). Insects Micronesia 4:13-30. Barnard, K. H. 1958. Terrestrial isopods and amphipods from Madagascar. Mem. Inst. Sci. Madagascar, A, 12:67-111. - Ruffo (1958) believes Talitrus pacificus and T. decoratum are both synonyms of T. topitotum; Bousfield and Carlton (1967) treat pacificus as a synonym of topitotum. I believe they are probably right, but prefer, like Ruffo, to keep the identities separate until the types have been compared. If the species are synonymous, topitotum has a wide Indo-Pacific distribution: India, Ceylon, Australia, Marquesas, Norfolk Island, Reunion, Comores, Madagascar, U.S.A. 351 Barrois, T. 1888. Note sur l'histoire naturelle des Azores. - De 1'adaptation de YOrchestia littorea Montagu a la vie terrestre. Bull. Soc. Zool. France 13:19-22. Birch, L. C, and D. P. Clark. 1953. Forest soil as an ecological community with special reference to the fauna. Quart. Rev. Biol. 28:13-36. Bolin, R. L. 1967. From the log of the "Te Vega." Natural History, (New York) 76:24-31. Bousfield, E. L. 1957. Notes on the amphipod genus Orchestoidea on the Pacific Coast of North America. Bull. S. Calif. Acad. Sci. 56: 119-129. Bousfield, E. L. 1964. Insects of Campbell Island. Talitrid amphipod crustaceans. Pacific Insects Monogr. 7:45-57. Bousfield, E. L., and J. Carlton. 1967. New records of Talitridae (Crustacea: Amphipoda) from the Central Californian Coast. Bull. S. Calif. Acad. Sci. 66:277-284. Bousfield, E. L., and W. L. Klawe. 1963. Orchestoidea gracilis, a new beach hopper (Amphipoda: Talitridae) from Lower California, Mexico, with remarks on its luminescence. Bull. S. Calif. Acad. Sci. 62:1-8. Bowers, D. E. 1964. Natural history of two beach hoppers of the genus Orchestoidea (Crustacea: Amphipoda) with reference to their complemental distribution. Ecology 45:677-696. Bulycheva, A. I. 1957. [Marine fleas of the seas of USSR and surounding waters]. Opred. Faune SSSR. 65:1-186. (MS translation by T. Pidhayny, Foreign Languages Division, Dept. of Canada; kindly lent by Dr. E. L. Bousfield). Chevreux, E. 1888. Sur quelques Crustaces Amphipodes recueillis aux environs de Cherchell. Compt. Rend. Assoc. Fr. Avance. Sci. 17 (1):198; 17(2):343-353. Chevreux, E. 1893. Notes sur quelques Amphipodes mediterraneens de la famille des Orchestidae. Bull. Soc. Zool. France 18:124-128. Chevreux, E. 1900. Amphipodes provenant des campagnes de l'Hirondelle (1885-1888). Res. Camp. Sci. Prince Albert I, 16:1-195. Chilton, C. 1920. A small collection of Amphipoda from Juan Fernandez, p. 81-92. In Carl Skottsberg, [ed.], The natural history of Juan Fernandez and Easter Island, Vol. 3. Almquist and Wiksell, Uppsala. Chilton, C. 1921. Amphipoda. Fauna of Chilka Lake. Mem. Indian Mus. 5:519-558. Clark, D. P. 1955. The influence of body weight, temperature and season upon the rate of oxygen consumption of the terrestrial amphipod, Talitrus sylvaticus (Haswell). Biol. Bull. 108:253-7. Cullen, D. J. 1967. Submarine evidence from New Zealand of a rapid rise in sea level about 11,000 years B.P. Palaeogeogr., Palaeoclimatol., Palaeoecol. 3:289-298. Dahl, E. 1950. On some terrestrial amphipods from the Canary Islands and Madeira. Ark. Zool., ser. 2, 1:195-198. 352 DESMOND E. HURLEY Dahl, E. 1967. Land amphipods from the Azores and Madeira. Bolm Mus. Municip. Funchal. 21, art. 96:8-23. Darlington, P. J., Jr. 1965. Biography of the southern end of the world. Harvard Univ. Press, Cambridge. 236 p. Dell, R. K. 1955. The land Mollusca of Fiordland, South-West Otago. Trans. Roy. Soc. New Zealand 82:1135-48. Dendy, A. 1895. The cryptozoic fauna' of Australasia. Rept. Australian Assoc. Advance. Sci. (Brisbane) 6:99-119. De Sylva, D. H. 1959. Talitrus (Talitropsis) fernandoi, sp. n., a new amphipod from Ceylon. Ceylon J. Sci. Biol. Sci. 2:86-8. Dorsman, B. A. 1935. Notes on the life-history of Orchestia bottae Milne-Edwards. Inaugural Dissertation, Leiden. Dresel, E. I. B., and V. Moyle, 1950. Nitrogenous excretion of amphipods and isopods. J. Exptl. Biol. 27:210-225. Edney, E. B. 1951a. The body temperature of woodlice. J. Exptl. Biol. 28:271-280. Edney, E. B. 19516. The evaporation of water from woodlice and the millipede Glomeris. J. Exptl. Biol. 28:91-115. Edney, E. B. 1954. Woodlice and the land habitat. Biol. Rev. 29:185-219. Ekman, S. 1953. Zoogeography of the sea. Sidgwick, Jackson, London. 417 p. Evans, J. W. 1958. Insect distribution and continental drift, p. 134-161. In S. W. Carey, [convenor], Continental drift, a symposium. Geology Dept., Univ. Tasmania, Hobart. Fleming, C. A. 1962. New Zealand biogeography. A paleontologist's approach. Tuatara 10:53-108. Florin, R. 1963. The distribution of conifer and taxad genera in time and space. Acta Horti Bergiani 20:121-312. Forster, R. R. 1954. The New Zealand harvestmen (Suborder Laniatores). Canterbury Mus. Bull. 2:1-329. Cuerne, J. de. 1887. Notes sur la faune des Acores. Diagnoses d'un mollusque, d'un rotifere et de trois crustaces nouveaux. Naturaliste, se>. 2, 9:194-195. Guerne, J. de. 1888a. Remarques au sujet de VOrchestia chevreuxi et de l'adaptation des araphipodes a la vie terrestre. Bull. Soc. Zool. France 13:59-66. Guerne, J. de. 1888b. Campagnes scientifiques du yacht Monegasque l'Hirondelle. Troisieme ann£e, 1887. Excursions zoologiques dans les iles de Fayal et de San Miguel. (Acores). GauthierVillars, Paris. Guerne, J. de. 1889. Les Amphipodes de l'interieur et du littoral des Acores. Bull. Soc Zool. France 14:353-360. Harrington, H. J. 1962. Paleogeographic development of South America. Bull. Am. Assoc. Petrol. Geol. 46:1773-1814. Harrington, H. J., and B. L. Wood. 1958. Quaternary andesitic volcanism at the Solander Is- lands. New Zealand J. Geol. Geophys. 1:419-31. Hatch, E. J. 1949. Studies on the fauna of Pacific Northwest greenhouses (Isopoda, Coleoptera, Dermaptera, Orthoptera, Gastropoda). J. New York Entomol. Soc. 57:141-165. Hurley, D. E. 1957. Terrestrial and littoral amphipods of the genus Orchestia, Family Talitridae. Trans. Roy. Soc. Xew Zealand 85:149-199. Hurley, D. E. 1959. Notes on the ecology and enviionmental adaptations of the terrestrial Amphipoda. Pacific Sci. 13:107-129. Hynes, H. B. N. 1955. The reproductive cycle of some British fresh-water Gammaridae. J. Animal Ecol. 24:352-387. Ingle, R. W. 1958. A new British record of the amphipod, Talitrus (Talitroides) sylvaticus (Haswell). Ann. Mag. Nat. Hist. ser. 13, 1:591-2. Kraepelin, K. 1900. Ueber die durch den Schiffsverkehr in Hamburg engeschleppten Tiere. Mitt, naturh. Mus. Hamburg 18:185-209. Lawrence, R. F. 1953. The biology of the cryptic fauna of forests. With special reference to the indigenous forests of South Africa. Balkema, Cape Town. 408 p. Lee, K. E. 1959. The earthworm fauna of New Zealand. Bull. New Zealand Dept. Sci. Indust. Res. 130:1-486. Mclntyre, R. J. 1954. A common sand-hopper. M.Sc. Thesis, Canterbury Univ., Cluistchurch. N. Z. Menard, H. W. 1964. Marine geology of the Pacific. McGraw-Hill, Inc., New York. 271 p. Mokievsky, O. B. 1949. Fauna of unconsolidated grounds in the littoral of. the West Crimea. Trudy Inst. Okeanol. 4:124-159. Nakata, S. 1961. Some notes on the occurrence of Phasmatodea in Oceania. Pacific Insects Monogr. 2:107-121. Palmen, E. 1949. Talitroides alluaudi (Chevreux) (Amphipoda, Talitridae) in Finnland gefunden. Arch. Soc. Zool. Bot. Fenn. 'Vanamo,' 2(1947):61-64. Platzman, S. J. 1960. Comparative ecology of two species of intertidal amphipods: Talorchestia megalophthalma and Orchestia agilis. Biol. Bull. 119:333. Paulian, R. 1961. La zoogeographie de Madagascat et des iles voisines. Faune Madagascar 13:1-481. Quate L. W. 1961. Zoogeography of Pacific Psychodidae (Diptera). Pacific Insects Monogr. 2:123-127. Ruffo, S. 1958. Amphipodes terrestres et des eaux continentales de Madagascar, des Comores et de la Reunion, (fitudes sur les Crustaces Amphipodes - L). M6m. Inst. Sci. Madagascar, ser. A, 12:35-65. Sachs, I. (Zaks, I. G.). 1929. [On the bottom communities of the Shantar Sea.] Izv. Tikhookean. Xauchno-promysl. Sta. 3:1-93. Sexton, E. W. 1924. The moulting and growth stages of Gammarus, with descriptions of the normals and intersexes of G. chevreuxi. J. Mar. Biol. Assoc. U. K. 13:340-401. TRANSITION TO LAND IN AMPHIPODS Sexton, E. W. 1928. On the rearing and breeding of Gammarus in laboratory conditions. J. Mar. Biol. Assoc. U. K. 15:33-55. Smallwood, M. E. 1903. The beach flea: Talorchestia longicornis. Cold Spring Harbor Monogr. 1:1-27. Smallwood, M. E. 1905. The salt-marsh amphipod: Orchestia palustris. Cold Spring Harbor Monogr. 3:1-21. Stock, J. H., and A. E. M. H. Bloklander. 1952. Notes on adventive Amphipoda (Crustacea, Malacostraca) on the Dutch Coast. Beaufortia 10:1-9. 353 Taylor, N. H. 1953. The ecological significance of the Central North Island ash showers. The soil pattern. Proc. New Zealand Ecol. Soc. 1:11-12. Waterhouse. F. L. 1955. Microclimatological profiles in grass cover in relation to biological problems. Quart. J. Roy. Meteorol. Soc. 81:63-71. Wieser, W. 1967. Conquering terra firma: the copper problem from the isopod's point of view. Helgolander Wiss. Meeresuntersuch. 15:282293. Williamson, D. I. 1951. On the mating and breeding of some semi-terrestrial amphipods. Rep. Dove Mar. Lab., ser. 3, 12:49-62.