AMER. ZOOL., 32:428^137 (1992)
Water and Solute Balance in the Transition to Land1
THOMAS G. WOLCOTT
Department of MEAS, North Carolina State University, Raleigh, North Carolina 27695-8208
SYNOPSIS. Terrestrial crabs are physiologically rather similar to their
aquatic relatives, despite their markedly different access to water and ions.
They have high evaporation rates and void vital salts in isosmotic urine.
Some of them manage to have fairly miserly water and ion budgets, but
others succeed despite profligacy. There is no single solution to the challenges of terrestrial life; each pairing of animal and environment must be
seen as a system in which a unique suite of behaviors compensates for
limited physiological prowess. By exploiting temporal and spatial variability of available microhabitats, each species assembles a "composite
habitat" in which it can balance the "debit" sides of its water and ion
budgets with the requisite "credits."
the temporal complexity of land crab microenvironments, the importance of behavIn leaving the stable and predictable ioral adaptations, and the variety of soluwomb of the sea for the fringes of land, crabs tions to environmental challenges.
Crabs are not obviously "preadapted" for
encountered new physiological challenges:
evaporation; some reduction (small or great) colonization of land. They lack a well-orgain access to free water; and in almost all nized lipid layer in the epicuticle, leading
terrestrial environments, where the sources to high rates of evaporative water loss. They
of water are fresh, a drastic reduction in rely on gills, which tend to collapse in air
and thus lose effective gas-exchange area.
access to ions.
Limited abilities to cope with the ensuing The resultant inefficiency obliges airproblems of water, ion and nitrogen balance breathing crabs to increase ventilation and
probably are the main factors preventing (presumably) evaporation. A third limiting
crabs from colonizing land as successfully factor is the excretory organs, which cannot
as insects and chelicerates. Peter Greenaway produce urine differing greatly from hemorecently (1988) reviewed the subj ect in Biol- lymph in total concentration. Under the
ogy of the Land Crabs, and Donna Wolcott hypo-osmotic conditions expected in most
(1991a) surveyed the cellular and subcel- terrestrial habitats (access to fresh water
lular phenomena involved. I am greatly only), voiding urine isosmotic to hemoindebted to their work, and since I can lymph would cause rapid loss of ions. Furnitrogen at
scarcely improve upon their thorough and thermore, aquatic crabs excrete
+
the
gills
as
NH
and/or
NH
;
on
land,
dilut3
4
insightful treatments, in this more abbreviated format I will attempt to give a concise ing these toxic substances would require high
overview and emphasize developments of rates of water expenditure.
the last few years, without exhaustive citaOn the other hand, crabs also have chartions. Because little has appeared on the acteristics that make them more suited than
endocrine control mechanisms for water and many other invertebrates for colonization
salt balance since the work of Dorothy Bliss of land. Freshwater crabs in particular are
and her colleagues, my focus will be at the armored by an exoskeleton relatively
whole-animal level. My main themes are impermeable to water and ions. Many species from brackish and fresh waters have
powerful ion transport systems that could
1
From the Symposium on The Compleal Crab pre- assist in maintaining ion balance.
sented at the Annual Meeting of the American Society
What is the principal challenge for crabs
of Zoologists, 27-30 December 1990, at San Antonio,
attempting to maintain water and ion balTexas.
THE PROBLEMS FOR CRABS
INVADING LAND
428
WATER AND SOLUTE BALANCE
ance in terrestrial habitats? It has become
clear in recent years that there is no single
answer. Each species lives in at least two
spatially and/or temporally separate habitats, typically foraging in one and using
another for refuge from physical (and biotic)
risks. The characteristics of those microenvironments, how crabs partition their time
between them, and the crabs' suites of adaptations to each, must be considered in judging degrees of terrestriality.
Thus, to understand water and ion balance of a given species, both the income and
debit sides of its water and ion budgets need
to be examined in light of its natural history.
Accordingly, I will present the major routes
of loss and gain, and examples of how some
of the better-known species play them off
against each other to maintain homeostasis
in their particular sets of microenvironments.
WATER BALANCE
Let us first consider the "Debit" side of
the water budget: the routes and rates of
water loss. Paramount are transcutaneous
(evaporative) and excretory losses.
Given the importance of evaporative
water loss, it is disappointing that so few of
the data collected on terrestrial species allow
interspecific comparisons. Few studies have
used ecologically and physiologically realistic conditions of water potential gradient
and airflow, based on field observations of
the microclimates crabs actually experience.
Despite these limitations of the data,
interspecific differences can be discerned.
There is a trend toward lower integumental
permeability with increasing terrestriality,
with the lowest permeabilities among the
Potamoid "freshwater land crabs" (Greenaway, 1988). The evaporation rates of most
terrestrial crabs are only 5-50% those of
aquatic crabs, similar to those of terrestrial
isopods, myriapods and insects from moist
environments, but still about 3-5 times those
of mesic/xeric insects, reptiles and mammals. Most anomurans are even more permeable than aquatic brachyurans, presumably because of the relatively thin
integument of the abdomen, but the highly
terrestrial Coenobitid hermit crabs and the
429
coconut crab Birgus latro are comparable to
terrestrial brachyurans (Harris and Kormanik, 1981).
It is not clear what proportion of evaporative losses is from the general body surface, and how much is from the respiratory
membranes. By selectively applying water
barriers (petroleum jelly), Herreid (1969a)
attributed 58% to the external surfaces (21%
legs, 22% body, 15% chelipeds). Dead animals have been used to estimate respiratory
water losses (Herreid, 19696) but Innes et
al. (1986) observed no marked changes in
evaporation rate when Cyclograpsus lavauxi
died, suggesting that ventilation adds little
to losses caused by diffusion of water vapor.
Use of masks or other means to capture
water lost in expired air would lay these
questions to rest.
There is little evidence that evaporation
from respiratory surfaces is an important
contributor to desiccation, yet this is commonly cited as the advantage of two structural modifications that recur among terrestrial crabs: gills tend to be smaller in more
terrestrial forms, and to be relegated to the
role of ion- and acid-base regulation
(Greenaway et al, 1988; Taylor and Innes,
1988). Thin, vascularized walls of the
expanded branchial chambers assume
responsibility for efficient aerial gasexchange (Diaz and Rodriguez, 1977; Taylor and Greenaway, 1984; Innes and Taylor,
1986; Taylor and Innes, 1988; Greenaway
etal, 1988).
Structural differences in exoskeletons that
contribute to the interspecific differences in
evaporative losses remain unclear. It is not
simply a matter of thickness or mineralization; Herreid (1969a) found that losses
through arthrodial membranes are minor,
and even heavily calcified exoskeletons may
have abundant pore canals (Roer, 1980) and
high permeabilities to water.
Behavioral reduction of transcutaneous
losses is achieved by escaping drying conditions in space or time. Most terrestrial
crabs burrow, providing themselves a humid
environment as well as physical protection.
Burrows in heavy clay allow Holthuisana
transversa in arid northeastern Australia to
survive months to years without rain
(MacMillen and Greenaway, 1978). A per-
430
THOMAS G. WOLCOTT
tipes given access to fresh water (the normal
situation) produced urine at 8.59% body
weight/day (Greenaway, 1989)—about 3
times higher than Cardisoma carnifex tested
on 80% seawater-dampened sand (Kormanik and Harris, 1981). Urine production
also depends on water availability. Under
desiccating conditions urine becomes difficult to collect, and inulin clearance ceases
in Gecarcoidea lalandii and Cardisoma carnifex (Harris and Kormanik, 1981). This reemphasizes the importance of using ecologically realistic experimental conditions in
the laboratory, based on field measurements.
On the "credit side" of the water budget,
there are several potential sources that crabs
could exploit. Those offering small amounts
include airborne water vapor, metabolic
Gecarcinus lateralis in dune hammock water, and preformed water in food. None
thickets; Bliss et al, 1978). Ghost crabs are of these seems likely to make a major conglaring exceptions to this generality; tribution. Water potentials of crabs are
although they forage mostly at night, in pop- comparable to that of air above 98% relative
ulations on undisturbed beaches many are humidity (Greenaway, 1988), making direct
active during the day when sand surface uptake of water from the vapor phase (as in
temperatures may exceed 40°C (T. Wolcott, some insects) improbable. Crabs (especially
1988, unpubl. obs.).
when desiccated) have low metabolic rates
Seasonally adverse conditions may be that yield minor amounts of metabolic
"escaped" by entering an inactive state. water.
Some highly terrestrial species lower their
It also appears that only carnivorous land
metabolic and ventilatory requirements by crabs could rely on preformed water in their
40-90% under desiccation stress, presum- diet. Many of the most terrestrial species
ably contributing to their very low evapo- are herbivorous or detritivorous; their conrative losses: e.g., Cardisoma carnifex sumption and assimilation rates are limited
(Wood et al, 1986), Holthuisana transversa by gut volume (D. Wolcott and T. Wolcott,
(MacMillen and Greenaway, 1978), and 1984). Consuming succulent foods would
Pseudothelphusa garmani (Innes and Tay- increase water intake, but at the expense of
lor, 1986; Taylor and Innes, 1988).
energy yield. Furthermore, as Donna WolUrine is the other major route of water cott discusses elsewhere in this symposium,
loss, and when crabs can avoid severely des- fresh vegetation often contains higher coniccating conditions it probably dominates centrations of defensive compounds than
the negative side of the budget. Interspecific does aged litter. In the laboratory, Cardicomparisons show a general trend toward soma guanhumi prefer dry or partially
lower rates of urine flow with increasing ter- decayed leaves to fresh (D. Wolcott and T.
restriality (Greenaway, 1988), from 2-4 ml • Wolcott, 1987), and the predominant items
100 g~'d~' for crabs of marine/estuarine in the diet of Bermudian G. lateralis are
origin to about 0.5 ml-100 g~'d~' for fresh- grass and dry needles of Casuarina equisewater land crabs. As with evaporation, some tifolia (D. Wolcott and T. Wolcott, 1984).
data are not truly comparable because of Water lost via feces may exceed that
differences in technique; some species have acquired in food.
been tested under conditions strongly hyThese "minor" water sources will properosmotic to what they probably encoun- vide a significant portion of the water budter in nature. For instance, Cardisoma hir- get only where the rates of water loss are
manent pool of free water exists in burrows
that extend below shallow water tables
{Cardisoma spp., Ucides cordatus). Under
dense vegetation, a few species may forego
burrowing to shelter in crevices or under
rocks and logs (Gecarcinus ruricola, Birgus
latro).
Temporal escape from desiccating conditions is accomplished by behavioral
rhythms, on several time scales. Intermittent ventilation of the branchial chambers
is sufficient, due to the high availability of
oxygen in air and the efficiency of crab
"lungs" (Greenaway et al, 1983; Innes et
al, 1987); periodic "apnea" may reduce
respiratory evaporation. On a diel scale,
most terrestrial crabs are nocturnal or crepuscular, except where heavy cover raises
humidity and lowers heat loading (e.g.,
WATER AND SOLUTE BALANCE
vanishingly small. "Estivating" Holthuisana transversa in humid clay burrows may
fit this description. Calculated from data in
MacMillen and Greenaway (1978) and
Greenaway and MacMillen (1978), a 10 g
hydrated crab could evaporate about 100
mg water daily. It could gain 2.4-7.2 mgd"1 (depending on dehydration and respiration rate) by metabolizing fat (RQ = 0.67).
During the night, up to 70 mg of water could
be gained by condensation each time the
crab re-entered the warm, humid burrow
depths after cooling 4CC at the burrow
mouth. The modest intake from condensation is sufficient to maintain, or even
increase, hydration (Greenaway and
MacMillen, 1978).
Sources for large amounts of water include
free surface water, precipitation, interstitial
water in soil, and groundwater in burrows
reaching the water table. Crabs can partially
immerse themselves in streams or puddles
and raise water into the branchial chambers
by scaphognathite pumping, or bring drops
directly to the mouth with the chelae. Most
species also have hydrophilic setal tufts that
conduct surface water (dew, raindrops) into
branchial chambers (Greenaway, 1988).
In ghost crabs and fiddler crabs (Ocypodidae), these setal tufts are large and also can
be used to draw water from capillary spaces
of soil. Scaphognathite pumping produces
sufficient negative pressure (as much as 76
mm Hg below ambient) to suck the water
into the branchial chambers, whence it can
be absorbed by gills or transferred to the
mouth and drunk (T. Wolcott, 1984;
Thompson et al, 1989). This method is only
feasible in relatively coarse-grained sediments with low organic and clay fractions;
others bind water too tightly (strictly, have
too negative a matric water potential) for
crabs to suck any out. This limits ghost crabs
to clean sandy sediments where they can
burrow to within a meter of the water table.
Similarly, species dependent on a pool at
the bottom of the burrow (Cardisoma spp.,
Ucides cordatus) may penetrate far inland,
but only where groundwater lies within
about 1.5 m of the surface.
It has been argued that the more terrestrial species reduce risk of desiccation by
having larger water stores, either in the sense
431
of a higher body water content or a higher
proportion of body water that may be lost
without damage. In fact, there is little evidence for such a trend. Total body water
(unfortunately seldom corrected for weight
of exoskeleton mineralization) is around 6070% in both terrestrial and aquatic species.
Tolerable loss shows no clear trends either,
lying in the range of 10-34% total body water
regardless of habitat. Holthuisana transversa stands out by having both a somewhat
higher body water and a higher tolerable
water loss (about 50%), but so do some
intertidal hermit crabs (Greenaway, 1988).
Short-term storage of fluid for molt increments is seen in species that molt without
access to water, like Gecarcinus lateralis
(Bliss, 1963; Mason, 1970) and Ocypode
cordimana (Rao, 1968). Hemolymph volume increases during premolt, the excess
being accomodated in swollen pericardial
sacs until ecdysis and then being used to
expand the new exoskeleton.
EXCRETION OF NITROGENOUS WASTES
Aquatic crabs excrete NH 3 and/or NH 4 +
via the gills; toxicity has been thought to
preclude excretion of these compounds
without extensive dilution. On land, the
supply of water for flushing the gill chambers is restricted. Recent studies have
revealed an ever-increasing variety of adaptations that permit crabs to circumvent this
dilemma.
One solution is to suspend production of
nitrogenous waste during desiccation. Cardisoma carnifex seems to shut down production of NH 3 (Wood et al, 1986). This
may be achieved by ceasing protein catabolism. More likely, it represents temporary
storage of NH 3 in some non-toxic form; at
the beginning of rehydration, ammonia
concentrations in hemolymph rise 4-6 fold,
and rates of NH 3 excretion increase 3-4 fold.
Another way to reduce the volume of
water required for excretion is by extrarenally loading branchial chamber water with
nitrogenous wastes. In Gecarcinus lateralis
under drying conditions, the source of branchial chamber water is urine, which contains only minute quantities of NH 4 + . At
the gills, enough NH4+ is added to increase
total nitrogen content 10-fold before the crab
432
THOMAS G. WOLCOTT
discards the "final excretory product," or
" P " (D. Wolcott, 1991*). Gecarcoidea
natalis behaves similarly, extrarenally
increasing urine NH4+ from 0.36 mM/liter
to an average of 11 mM/liter (max. of 73
mM/liter); the ammonia in " P " accounts
for 68% of the crabs' nitrogen output (Greenaway and Nakamura, 1991).
A third option is uricotely: excreting, or
storing, nitrogenous wastes as insoluble,
non-toxic uric acid. Crabs have been thought
to lack the biochemical machinery to synthesize uric acid de novo, yet several species
of Gecarcinid and highly terrestrial Ocypodid land crabs contain extensive white
deposits that test positive for uric acid or
its salts (D. Wolcott and T. Wolcott, 1984;
Wood and Boutilier, 1985; Greenaway and
Morris, 1989). In C. guanhumi the quantity
of these deposits, particularly when the crabs
are fed an unnaturally high-protein diet, can
reach 16% of gross dry weight, or more than
half the ash-free (tissue) dry weight (Gifford,
1968). Because postmolt crabs seem to have
less of these deposits than premolt animals,
it has been suggested that they are somehow
voided or remobilized at the molt (Bliss and
Mantel, 1968; Wood and Boutilier, 1985;
L. H. Mantel, personal communication). We
have found that the deposits are usually laid
down around blood vessels as spherules a
few micrometers in diameter, and in our
laboratory, similar quantities occur in preand postmolt crabs. Reduced availability of
water seems to increase urate load 10 times
as much as increasing dietary nitrogen (D.
Wolcott and T. Wolcott, 1987). No examinations have been conducted of the deposits' histological relationship to surrounding
tissues, or their chemistry. It remains
unknown whether they serve any function
beyond "safe storage" of excretory nitrogen,
or even whether they are permanent.
Despite crabs' previously-reported
inability to synthesize purines, Birgus latro
recently has been shown to excrete 79.5%
of its waste nitrogen as urates, apparently
synthesized in the midgut gland (Greenaway and Morris, 1989). Urates are voided
in white feces that are produced every few
days, in contrast to the usual brown, uratefree feces.
Yet another option is excretion of gaseous
NH 3 , previously thought to be limited to
some terrestrial isopods. However, Geograpsus grayi excretes over 80% of its waste
nitrogen as NH3, released in bursts over 12 day periods alternating with similar periods of no NH 3 release (Greenaway and Nakamura, 1991).
All of these are ways to minimize internal
concentrations of NH 3 /NH 4 + . Because even
low ammonia levels are toxic (physiology
texts give values of a few micromolar to a
few millimolar, depending on species and
conditions), Greenaway and Nakamura
(1991) expressed reservations about a report
by Green et al. (1959) of 20 mMNH 4 + /liter
in hemolymph of Uca spp., and 75 mM/
liter in urine.
New data from Donna Wolcott's lab suggest that high ammonia concentrations may
be normal for some species. In comparing
nitrogen excretion across families, she and
Mona DeVries have found little ammonia
(as expected) in urine of herbivorous Gecarcinus lateralis or Cardisoma guanhumi; preliminary data also show low NH 4 + in hemolymph. The carnivorous ghost crabs
(Ocypode quadrata) yield strikingly different values. The hemolymph ammonia again
is low (0.54 mM, n = 7), but concentrations
of NH4+ and amines in the urine far surpass
those seen in any other species, averaging
212 mM (n = 10) with one sample reaching
445 mM. Concentrations on this scale suggest other functions for urine besides excretion (e.g., repelling predators, intraspecific
signalling, cleaning greasy windows). Some
preliminary data for Uca pugilator on a highnitrogen diet show 2.25 mMin hemolymph,
and high concentrations in urine (average
98 mM, n = 11; max. 220 mM). The urine
is extremely acidic (averaging pH 5.36,
minimum pH 4.7, n = 10), suggesting that
NH 3 is acid-trapped in urine as relatively
non-toxic NH4+ (M. C. DeVries and D. L.
Wolcott, personal communication). It seems
that at least some Ocypodids have evolved
mechanisms to produce, and tolerate,
extremely high concentrations of ammonia
instead of relying on "dilution as the solution to pollution."
ION BALANCE
Most land crabs have little or no contact
with seawater, except for reproduction. A
few species, like Uca subcylindrica (Rabalais
WATER AND SOLUTE BALANCE
and Cameron, 1985) and Cardisoma guanhumi (personal observation), may occupy
habitats where evaporation exceeds precipitation and both surface and groundwater
become hypersaline; their mechanisms of
hypo-regulation need further study. Most
land crabs contact only hypo-osmotic or
fresh water and must cope with salt shortage.
The "debit side" of the salt budget is
therefore particularly important. The principal routes of salt loss are urinary, transcutaneous (including across respiratory membranes) and fecal. The transcutaneous route
is likely to be significant only in species that
spend time immersed and provide opportunity for ions to diffuse from hemolymph
into hypo-ionic media. Such species (e.g.,
Cardisoma spp. with pools in their burrows,
or freshwater land crabs that are active in
streams) typically show reduced permeabilities to both ions and water. Cardisoma
hirtipes, which burrows around freshwater
seeps on Christmas Island (Indian Ocean),
has an Na+ permeability only l/20th that
of marine crabs, but still about three times
higher than that of freshwater land crabs
like Holthuisana transversa (Greenaway,
1989). No evidence exists for short-term
adjustment of permeabilities to ions in
response to physiological state. The extent
of diffusional losses through the integument
under field conditions is not known, because
the proportion of time spent immersed has
not been measured. A telemetric study of
position in burrows vs. time would shed light
on this issue.
Urine appears to be the principal route
of ion loss, even in the amphibious species.
The fact that these animals all have rather
high hemolymph concentrations, and urine
that is similar osmotically and ionically to
hemolymph, leads to large ion losses per
volume of urine. In Cardisoma guanhumi
and C. hirtipes immersed in fresh water, and
Birgus latro given access to seawater, urinary losses (calculated from clearance rates)
account for almost all of the Na+ lost (Kormanik and Harris, 1981; Greenaway, 1989).
Cardisoma carnifex loses 34 micromoles
NaVlOO g h r via urine in distilled water,
equivalent to about 0.3% of its hemolymph
Na+ (Kormanik and Harris, 1981).
Fecal ion losses probably are inconse-
433
quential. Feces are produced in quantity only
when crabs are feeding; concentrations of
salts in feces are low relative to those in
food, permitting net gains (T. Wolcott and
D. Wolcott, 1988).
On the "credit side" of the ion budget,
ion sources include environmental water and
food. Free water (precipitation, standing
water, streams, soil interstitial water, burrow water) are essentially fresh. Those species that spend time immersed have highafnnity, high-capacity ion transport pumps
in the gill membranes. Cardisoma guanhumi maintains steady state in 0.5-0.8 mM
Na+ (Herreid and Gifford, 1963); C. carnifex are "in equilibrium" with burrow water
containing 2-6 mM Na+, and readily take
up ions from 1% seawater (Wood and Boutilier, 1985). Cardisoma hirtipes from freshwater seep areas maintain sodium balance
in media containing only 0.12 m # N a + , and
survive indefinitely at 0.5 m M N a + (Greenaway, 1989). Ion concentrations comparable to these can occur even in rain puddles
and dew drops in the field (T. Wolcott and
D. Wolcott, 1988). Assuming that Cardisoma spp. urinate into the limited volume
of their pools, Greenaway (1988) suggested
that ions accumulate to levels permitting
recycling for osmo- and ion-regulation. Field
data are lacking about where crabs actually
release urine, and about the exchange rate
of burrow water with the surrounding water
table. There are reasons to doubt that crabs
urinate into the pool (see discussion of urine
recycling, below).
Dietary contributions to the ion budget
will differ greatly, depending on whether a
species is carnivorous or herbivorous. Ghost
crabs (Ocypode quadrata) have a diet that
is 90% osmoconforming invertebrates (T.
Wolcott, 1978), providing ions in abundance. In contrast, Gecarcinus lateralis and
Cardisoma guanhumi subsist largely on leaf
litter and grass, which provide relatively few.
Furthermore, the ionic ratios of vegetation
differ from those of crabs, potentially leading to shortages of some ions (e.g., Na+) and
overabundance of others (e.g., K+, Ca + + ,
Mg + + ; Wood and Boutilier, 1985; T. Wolcott and D. Wolcott, 1988).
Given that the principal environmental
challenge is hypo-ionic conditions, the principal adaptations influencing ion budgets are
434
THOMAS G. WOLCOTT
those that minimize losses. Transcutaneous
losses can be avoided simply by minimizing
contact with dilute water, or, for hermit
crabs, by filling the adopted shell with an
appropriate mixture concocted from available salinities. Fecal losses can be cut by
reducing the volume and concentration of
fluid in the feces. Gecarcinids typically produce compact feces containing low amounts
of salts (T. Wolcott and D. Wolcott, 1988).
Information is lacking for other species.
Urine is undoubtedly the major route of
salt loss in most land crabs, and mechanisms that reduce urinary loss have the most
impact on ion budgets. Reducing the volume of urine produced is not an option when
salt shortage is caused by water loading from
hypo-osmotic media. It would be expected
that crabs immersed in fresh water would
have higher urine production rates than
those that could regulate their contact with
the water; surprisingly, this made no difference to Cardisoma hirtipes (Greenaway,
1989). However, these crabs were fed and
the ion contributions from food may have
forestalled induction of ion-conservation
behaviors.
Limitations of the excretory organs prevent reducing concentration of the urine
below that of hemolymph. However, a subaerial existence presents the option of passing originally isosmotic urine to organs that
can pump ions against large gradients (gills,
perhaps gut). When Ocypode quadrata,
Gecarcinus lateralis, or Cardisoma guanhumi are loaded with water to force urine
production, but depleted of salts, they still
produce isosmotic urine. Instead of being
discarded, this urine is passed into the branchial chambers and modified. The final
excretory product ("P") discarded by the
crabs is hypo-osmotic to hemolymph. Much
of the difference is due to reduction (often
>90%) in Na + and Cl~ (T. Wolcott and D.
Wolcott, 1984, 1985, 1991, and in preparation). Dye tracing suggests that the gills
are the site of urine reprocessing; there is
no indication that the gut is involved (T.
Wolcott and D. Wolcott, in preparation).
Marking with inulin indicates that dilution
of the urine is accomplished by resorption
of Na + and Cl~, and part of the water. The
net result may be reclamation of over 95%
of the NaCl in the urine (T. Wolcott and D.
Wolcott, 1984, and in preparation). Thus
urine, as the most concentrated salt solution
available, becomes a valuable recyclable
waste. Gecarcinus lateralis rapidly experiences hemodilution when denied the option
of recycling urine (D. Wolcott, 1991 b); when
permitted to do so, it conserves ions so
effectively that their availability does not
appear to affect the limits of landward distribution (T. Wolcott and D. Wolcott, 1988).
Urine reprocessing appears to be a common phenomenon among land crabs. In
Birgus latro, actual Na+ loss was far less than
that predicted from clearance rates (Kormanik and Harris, 1981), suggesting ion reclamation. Subsequent work has provided
additional evidence for recycling in Birgus
(Greenaway and Morris, 1989) and Gecarcoidea natalis (Greenaway and Nakamura,
1991).
Urine recycling functionally allows crabs
to produce a dilute excretory fluid, giving
them a common advantage with the terrestrial vertebrates possessing "good kidneys."
The decoupling of water and ion fluxes is
probably one of the major advances allowing the land crabs to penetrate environments where water sources are strongly
hypo-osmotic.
Land crabs do not appear to have any
remarkable mechanisms for storing ions,
despite the low and unpredictable supplies
in their environments (Greenaway, 1988).
Compared with aquatic crabs, they store little more of their exoskeletal minerals (about
10%) when molting, but in a sense store
some extracorporeally by molting in refuges
(burrows) and, once the mouthparts are sufficiently hardened, consuming much of the
old exoskeleton. Some species store calcium
as gastroliths during premolt skeleton demineralization, but there is not a clear correlation with habitat. Holthuisana transversa, which may spend months to years
without access to dietary or aquatic sources
of ions, has another unique adaptation, storing 65% of its exoskeletal calcium as spherules suspended in the hemolymph (Sparkes
and Greenaway, 1984). Insoluble urate salts
are a potential depot of cations, but whether
435
WATER AND SOLUTE BALANCE
DIURNAL
BEACH
BURROW IN
DAMP SAND
High Permeability
High Evaporation
Rapid Uptake of
(Fresh) Soil Water
Flexible Ion Conservation
(Urine Recycling)
High-ion Food
Access to SW
NH3/NH4+-loaded Urine
High-Nitrogen
Food
BURROW
REACHING
GROUNDWATER
DRY, SHADED
:=> TERRAIN
Moderate Permeability
Moderate Evaporation
Freshwater Pool
in Burrow
Low-Ion (Plant) Diet
No Access to SW
Flexible Ion Conservation
(Urine Recycling)
Sequestration of Urates
Low-Nitrogen (Plant) Diet
Low Excretory Water Loss
BURROW
(DRY SOIL,
HUMID ADI)
DRY,
SHADED
TERRAIN
Refuge from
Desiccation
Low Permeability
Low Evaporative Losses
Crab inactive,
"closed system"
Low, Unpredictable
Availability of (Fresh) Water
Very Effective Ion
Conservation (Urine Recycling)"
N-Load "P"
±
Sequestration of «-^ (Drought)
Urates
*" -
Low-Ion
(Plant) Diet
Low-Nitrogen
(Plant) Diet
FIG. 1. Representative terrestrial crabs that maintain water and solute balance with differing turnover rates,
a. High-turover: Ghost crabs (Ocypode quadrata). By extracting soil interstitial water from a benign microenvironment (the burrow), this high-evaporation species also can exploit the diurnal beach surface, one of the
hottest (>40°C) and driest microhabitats experienced by any terrestrial brachyuran. b. Moderate turnover:
Cardisoma spp. Use of burrow water allows maintenance of water and solute balance even with long daily
activity periods; the latter may be necessary for growth and reproduction because the diet is of poor quality (D.
Wolcott and T. Wolcott, 1984, 1987). c. Low turnover Gecarcius lateralis. No water is available from dry
burrow soil; that above ground is typically so limited that, despite low evaporation rates, the crabs can afford
to be active only when humidity is high. The restrictions on feeding time, coupled with a low-quality (vegetarian)
diet, may limit growth rates.
436
THOMAS G. WOLCOTT
the extensive white deposits in some land spatial and temporal "composite habitat"
crabs serve any such function awaits chem- within which it can maintain homeostasis.
ical analyses.
Consequently, as we seek to more fully
understand water and ion balance in the
BALANCE OF WATER AND SALT BUDGETS
transition to land, we should abandon the
In the context of this review, the criterion notion that species occupy different stations
of "successful adaptation" to terrestrial on a continuum of "terrestriality." Instead,
environments is balance of water and ion we need perceptive field work to discover
budgets, not the absolute turnover rates. For how, where and when these fascinating aniinstance, high evaporative losses are not mals are doing their living in nature. Only
detrimental if the crab also has a mecha- then can we be assured that future comparnism that permits large gains of water; con- ative studies in the laboratory will ask the
versely, low rates of ion acquisition are tol- right questions and yield ecologically releerable if the animal is able to keep ion losses vant information.
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