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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)
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