Behavioral Regulation of Hemolymph Osmolarity Through Selective Drinking in Land Crabs, Birgus latro and Gecarcoidea lalandii

8 Pages·1992·3.5 MB·English

by  C A Combs

Reference: Biol Bull 182: 416-423. (June, 1992)
Behavioral Regulation of Hemolymph Osmolarity
Land
Through Selective Drinking in Crabs,
Birgus latro and Gecarcoidea lalandii
CHRISTIAN A. COMBS, NICOLE ALFORD, ANGELA BOYNTON,
MARK DVORNAK, AND RAYMOND HENRY
P.
Department ofZoology and Wildlife Science. 101 Cary Hall, Anbwn University, Alabama 36849
Abstract. Drinkingbehavior in Birgus latroand Gecar- physiological, and behavioral strategies were required to
coidea lalandii was videotaped under controlled labora- overcome the barrier ofdesiccation and concomitant in-
tory conditions. B. latro displayed the drinking behavior crease in hemolymph ion concentrations. Changes in he-
typically observed in nature, spooning up water with the molymph ion concentrationscan profoundlyaffect many
chelae (Lister, 1888; Gross, 1955). G. lalandii is docu- physiological processes in crustaceans including respira-
mented for the first time displaying this same behavior; tion, acid-base status, intracellular fluid volume, nitrog-
however it obtained water primarily through immersion. enous waste elimination, and enzyme function (Harris,
Under normal hydrated conditions (hemolymph osmo- 1977; Burrgren and McMahon 1981, 1988; Morris el al.,
larities < 1050 mOsm) B. latro showed no preference for 1988; Wheatly et al.. 1984; Wood el al. 1986; forreviews
drinkingfreshorseawater. Whendehydrated(hemolymph see Hugginsand Munday. 1968: Schoffeniels, 1976; Gilles
osmolarities > 1050 mOsm) B. latro altered its drinking andPequeux. 1981; Mangum, 1981; Taylor, 1982; Yan-
behaviorand showed adistinct preference for freshwater. cey et al.. 1982). In land crabs, dehydration and changes
This strategy resulted in restoration of original hemo- in hemolymph concentration are resisted using combi-
lymphosmolaritiesandwetweightsandwasaccomplished nations of adaptations such as immersion, burrowing,
through periods ofintensivedrinkingactivity. Conversely. water storage in the body or branchial chambers, evolu-
G. lalandii never experienced true dehydration; rather, tionary reduction in gill size, urine reprocessing, excretion
the hemolymph became hyperosmotic compared with of nitrogenous waste as urea or uric acid, and drinking
control animals. This species preferred freshwater both (Blissand Mantel, 1968; Bliss, 1979; Mantel and Farmer,
under normal and hemoconcentrated conditions. G. la- 1983; Powersand Bliss, 1983; WolcottandWolcott, 1985,
landiiwasalsoabletoosmoregulate behaviorallyandwas 1991; Greenaway, 1988; Greenaway et al.. 1988; T. G.
able to restore hemolymph osmolarities to normal con- Wolcott. 1988; D. L. Wolcott. 1991).
centrations via immersion in freshwater following exper- Drinking, or spooning up water with the chelae to the
imentally induced hemoconcentration. Possible physio- mouthparts, hasbeen documented in Gecarcoidea natalis.
logical and ecological reasons for the differences in water Geograpsus grayi. Cardisoma guanhiimi (Gross et al.,
uptake strategies and preferences are discussed. 1966), C. carnifex (Greenaway, 1988), Gecarcoidea lal-
andii(this paper), and in Birgus latro(Lister, 1888). Fresh
Introduction and seawater are available to most land crabs, but it is
not known precisely how the more terrestrial species use
The transition from the aquatic to the terrestrial en- the twoto regulate theconcentration oftheirhemolymph.
vironment wasboth problematic and beneficial forcrabs. These crabs inhabit islands in the Indo-Pacific region
Although oxygen was more readily available and there where rainfall is seasonal and water sources other than
were new resources to exploit, certain morphological. the ocean may become scarce at certain times of year
(Gross, 1964). This study examines the drinking prefer-
Received9 September 1991;accepted 26 February 1992. ence oftwo ofthe more strictly terrestrial crabs, Birgus
416
BEHAVIORAL OSMOREGULATION IN CRABS 417
latro (Anomura) and Gecarcoidea lalandii (Brachyura), concentrated conditions, allowingat least a48 h recovery
when hemolymph concentrations are normal and hemo- period between experiments.
concentrated (with possible dehydration). All crabs were allowed to adjust to the chambers for
24 h prior to observation/videotaping, while remaining
Materials and Methods on their water regime. Immediately preceding an obser-
vation period, crabs were weighed to the nearest 0.1 g on
Animal collection andmaintenance atoploadingbalance(Sartorius), andabloodsample(0.1
Specimens ofboth species, Birgus latro (500-2100 g) ml) was taken from the infrabranchial sinus. The water
and Gecarcoidea lalandii (65-220 g) were obtained from in each chamber was replaced with 225 ml of seawater
the islands of Palau and Pohnpei and were shipped via (35 ppt)and 225 ml offresh (deionized) waterwas placed
air-freight in damp burlap inside coolers or ice chests. randomly in either the right or left dish. The crabs were
Theyweremaintained in isolated Nalgenetanks(B. latro) then recorded for 12 h (1800-0600 h) using a Panasonic
or fabricated wooden pens with plexiglass partitions (G. VHS RecorderModel AG-HT3. After 12 h,thecrabswere
lalandii) in adark room at approximately 25 C. All were weighed, bloodsamplesweredrawn, andthewatervolume
fedcoconut, lettuce, and appleseven otherday, andwere remaining in each bowl was measured to the nearest 1.0
given either dechlorinated tapwater or seawater (35-40 ml. Evaporative waterlosswasquantified usingduplicate
ppt, as determined with a refractometer) depending on bowls of freshwater and seawater placed in an empty
chamber. Temperature and relative humidity were also
the subsequent testing regime.
recorded using a ExTech Instruments Digital Humidity/
Temperature Meter.
Protocol
Hemolymph samples were placed in microcentrifuge
Observation chambers were constructed using standard tubes and kept on ice. After being sonicated at 20 watts
75 and 1151aquaria fittedwith a falsebottom ofplexiglass for 10 s with a Microson Cell Disrupter CM-1 converter
to facilitate viewing and minimize water spillage. Two (Heat Systems Ultrasonics, Inc.), the sampleswerecen-
circular holes were cut side-by-side in the false bottom to trifuged for 1 min using a Micro-Centrifuge Model 235B
allow access to a pair of glass preparation dishes (115 (Fisher). Osmolarity was determined on 10 n\ samples of
X 50 mm. Fisher) that were secured with silicone to the serum usinga Wescor 5100C Vapor Pressure Osmometer.
aquarium floor. The tops of the dishes were flush with Quantification of the number of drinks, time spent
the plexiglass platform, simulating pools of water. The drinking, and timespent immersed in thewaterbowl were
chamberwasdarkened on threesidestoisolateeachcrab. determined from videotapeanalysis. An individual drink
The uncovered end of the aquaria permitted head-on was considered to be a cheliped sweep from the water to
viewing ofboth bowls. A plexiglass cover with air holes the mouth and subsequent sweep by the maxillae over
forventilation wassecured to each tank to prevent escape. the cheliped to remove the water (Lister, 1888). Time
Drinking behavior of animals was recorded for indi- spent drinking wasdesignated asthe time ofthe first che-
viduals displaying hemolymph osmotic concentrations liped sweep to the time of the last cheliped sweep. Im-
typically found for crabs sampled in the field (<1050 mersion time was considered to be the amount oftime
mOsm) (as reported by Henry and Cameron, 1981; that a crab had part ofits carapace submerged in a water
Greenaway, 1988) and after hemoconcentration with bowl.
possible dehydration (hemolymph osmolarity > 1050
mOsm). The former condition was maintained by allow-
Statistics
ingcrabstodrinkadlibitum from both fresh andseawater.
Hemoconcentration was achieved through a combination Paired /-tests were used to determine ifthere were dif-
ofwater deprivation and allowing access to only hyper- ferences between water preferences within hemolymph
saline water (>35 ppt). Animals were weighed daily and concentration treatments, weight differences between he-
were not allowed to lose more than 12% oftheir initial molymph concentrations, and starting and ending he-
wetweight, avaluethatwaswithin the maximal tolerable molymph concentrations between treatments. Analysis
levelsofdehydration as reported by Kormanik and Harris ofvariance(ANOVA)wasusedtodetermineiftherewere
(1981)and Burggren and McMahon (1981). Hemolymph differences between the preferences ofcrabs fordrinking
osmolality was measured concurrently to determine at freshwaterorseawaterbetween hemolymphconcentration
what point values exceeded 1050 mOsm, after which an conditions in each species. To reduce biases inherent in
experiment was begun. individual animals, only individuals that were tested at
Individual crabs were randomly assigned their initial both hemolymph conditions were included in the statis-
condition, normal orhemoconcentrated. Behaviorofeach tical analysis. Scheffe's multiplecomparisonstestwasused
individual was recorded under both normal and hemo- to compare means ofthe variables between normal and
418 C. A. COMBS ET AL.
hemoconcentrated treatments. All data were tested for centrated crabs exhibiting the same preference (Scheffe:
normality using the Wilkes-Shapiro test and can be as- P < 0.05). This behavior led to a significant difference in
sumedtobenormallydistributed unlessspecified. All sta- osmolarity changes before andafterthe 12-h testsbetween
tistical analyses were accomplished with the SAS sta- the normal and hemoconcentrated treatments (/-test: P
tistical computer package (SAS Inst., Inc., 1982). < 0.02), with the hemoconcentrated animals reducing
their average osmolarity by 18% to 948 26 mOsm. In
Results addition, differences in weight before and after the 12-h
tests were significantly different between control and
Strategies ofwater uptake hemoconcentrated animals(/-test: P< 0.01)with normal
The two species employed different strategies ofwater animals averaging only a 5 12 g weight gain while he-
uptake both to maintain a normal hemolymph osmotic moconcentrated animalsgained 75 16g(Fig. 1). There-
condition and to reduce hemolymph concentrations in fore, B. latro compensated for hemoconcentration via
response to hemoconcentration (often accompanied by watergain, indicatingthat initial hemoconcentration was
dehydration in B. latro). B. latro used cheliped drinking accompanied by dehydration.
as the only means of water uptake, spending 100% of All specimens of Gecarcoidea lalandii that began an
their drinking time in that behavior; immersion in the experiment in a normal hemolymph concentration state
waterbowlswas not employed, although the bowlscould (947 31 mOsm) were also able to maintain that state
haveaccommodated atleast portionsoftheirbodies. The over the 12-h observation period (/-test: P > 0.77) (Fig.
observeddrinking behaviorwas virtually identical tothat 3). On average, specimens of G. lalandii that began an
reported previously by Lister(1888). G. lalandii, however, experiment in a hemoconcentrated state (1168 27
was observed in cheliped drinking behavior only 2% of mOsm) were able to reduce their hemolymph concentra-
the time; the remainder ofthe time in contact with water tion back to control levels (/-test: P > 0.30) over the 12-
twhaeswsapteenrtbwoiwtlh. Walhleonr ptahrits sopfectiheescdairdaepnagcaegeimimnecrhseeldipeidn fherorbesderovvaetrionseapewraitoedr. aFtrebsohtwhateorsmwotaiscsisgtnaitfeisca(n/t-ltyestp:reP-
drinking, the behavioral pattern was similar to that seen < 0.05 and P < 0.1, respectively) when immersion time
was used as an indicator of behavioral osmoregulation
in B. latro.
(Fig. 4). Moreover, there is a significant difference in the
amount oftime spent immersed in seawater between the
Normal water uptake and response to
twoosmoticstates, with moretimebeingspent in seawater
hemoconcentration
when individuals started the experiments hemoconcen-
All specimens ofB latro that began an experiment in trated (ANOVA: P < 0.05, Scheffe: P < 0.05). The data
a normal hemolymph concentration state (848 22 for number of cheliped drinks and time spent cheliped
mOsm) were able to maintain that state over the 12 h drinking were not normally distributed, but freshwater
observationperiod(Mest:P>0.81)(Fig. 1). Undernormal was overwhelmingly preferred at both hydration states
conditions, B. latro spent an average of61 min engaged (Fig. 4) for the small amount of time, 2%, this species
in drinking, performing 660 individual cycles ofcheliped spent cheliped drinking. End-volume differences in the
sweepsduringa 12-hexperiment. Thisspeciesshowed no drinking bowls were not examined in this species due to
preference forfresh orseawater, eitherwith respect to the the propensity ofthe animals to splash water out ofthe
percent ofthe total drinks taken from each bowl (/-test: bowlswhileenteringandexitingfromthem. Thisobscured
P> 0.73), the time spent drinking from each bowl (/-test: anydifferencesthat mighthavebeenduetotheirdrinking
P> 0.2), orthe percent ofvolume that wasdrunk (/-test: orabsorbingwater. Differences inweight before andafter
P> 0.2) (Fig. 2). the 12-h tests were not significantly different between
When individuals were hemoconcentrated prior to an control and hemoconcentrated animals (/-test: P> 0.25).
experiment(1171 51 mOsm), both the overall drinking Therefore, G. lalandii did not compensate for hemocon-
behavior and the drinking preference were altered. Ani- centration by water gain but rather appeared to reduce
mals in a hemoconcentrated condition increasedtheirto- hemolymph ion concentrationsthrough ion exchangevia
tal drinking time by over four-fold to 273 min, takingan immersion in the ambient water.
averageof2702 individual drinksduringthattime. These
animals displayed a distinct preference for freshwater for Discussion
all threevariables measured: totaldrinks, timeofdrinking,
and volume consumed (Mest: P < 0.01) (Fig. 2). In ad- Both Birgus latro and Gecarcoidea lalandii can os-
dition, the drinking preferences were different between moregulate behaviorally, by selecting drinking water of
thetwoosmoticstates(ANOVA: P<0.01)withallcontrol theappropriatesalinity, underlaboratoryconditions. Us-
crabs exhibiting the same preference and all hemocon- ing this strategy they were able to maintain hemolymph
BEHAVIORAL OSMOREGULATION IN CRABS 419
1450 A DEHYDRATED
-~ 1J50
1150
X5* HYDRATED
i
1050
850
1UJ
.50
750
650
PH PH BO NA B5 Bl MA R2 B3 83 PH BO B5 Bl NC Bl B3
HYDRATED DEHYDRATED
B
2200 -
420 C. A. COMBS ET AL
than drinking, but because these recordings were unat-
DEHYDRATED tended it is unclearwhetherallthebehaviorrecorded was
i
actually drinking. Our study had the distinct advantage
I
HYDRATED ofdirectly viewing all ofthe animals' behavior, thereby
i allowing differentiation ofdrinking and exploratory be-
haviors, which enabled precise quantification ofdrinking
i behavior.
Birgn.*; Intro usually inhabits sand burrows or piles of
decaying vegetation during the day and forages at night
f when ambient temperatures are cooler (Gross, 1964).
These crabs employ both physiological and behavioral
means ofosmoregulation, although the main method ap-
fw sw fw sw pears to be behavioral avoidance of desiccation (Gross,
DEHYDRATED 1964)alongwith uptakeofwaterbydrinking from inland
pools. Birguslalroalso usesa suite ofphysiological adap-
3E- tions forosmoregulation. B. latrocan reabsorb salts from
HYDRATED the urine (Harris and Kormanik, 1981; Greenaway and
* Morris, 1989)and ithasevolvedtheabilitytoexcreteuric
acid and thereforewaste lesswaterin nitrogen elimination
(Bliss and Mantel, 1968: Kormanik and Harris, 1981;
Greenaway and Morris, 1989). During periods ofdehy-
dration, specimens ofB. latro continue to produce isos-
motic urine and maintain intracellular fluid volume while
sacrificing extracellular stores (Burggren and McMahon,
1981; Harris and Kormanik, 1981). The large abdomen
fw sw fw sw isthewaterstorage site in B. latro(Harrisand Kormanik,
- c DEHYDRATED 1981) and becomes quite distended when fully hydrated,
i butonlyasmall volumeofwaterisstoredin thebranchial
HYDRATED cavity relative to other terrestrial crabs (Wood and Bou-
tilier, 1985). In addition, the gills are highly reduced
f
(Cameron, 1981), thus limiting evaporative water loss,
and they are used as exchange sites for ions, water, and
i carbon dioxide with oxygen uptake taking place at the
primitive lung (Greenaway el ai, 1988). Thus, it seems
that B. Intro'sability todifferentiate between waterofdif-
i ferent salinities and its precise regulation ofhemolymph
concentration through piecemeal drinking augment its
suite ofother behavioral and physiological mechanisms
fw sw fw sw and help to explain its high degree ofterrestriality.
Figure 2. Drinkingpreference for freshwaterorseawateraccordingto Birgu\lalrohasneverbeen observeddrinkingseawater
initialhemolymphconcentration(hydratedanddehydrated)during 12- directly from the ocean, although tracks havebeen found
hourtestsinvolvingBirguslalro(n = 5). Drinkingpreferenceisexpressed on dunesclose to the shoreline (Gross, 1964), and Grubb
as (A) mean percentage oftotal drinks. (B) mean percentage oftotal 1971 reported anecdotal evidence ofcoconut crabs vis-
timespentdrinking, (C) mean percentage oftotal volumechangefrom (iting t)he ocean. Considering the evidence presented in
waterbowls(normalized forevaporativewaterloss). this study as well as in Gross (1955). B. Intro might use
theocean asawatersource undercertain conditions. Field
which the quantification ofthe drinking preference was studies investigating the natural behavior ofthese crabs,
obtained. Gross ( 1955) quantified drinking behavior in- particularly on some ofthe dry Pacific atolls, would help
directly. Drinking behavior was monitored by etchings bring the findings ofthis study into context with the nat-
made on Kymograph drums caused by depressions of ural strategies these animals employ to osmoregulate be-
platformsoverdrinkingbowls(seeGross, 1955, 1957 and haviorally.
GrossandHolland, 1960fordetails). Theseetchingswere Gecnrcoidea lalandii usually inhabits dry inland bur-
then used to quantify drinking bouts. Precautions were rows(Bliss, 1968) and probably relies on intermittent ac-
taken in his study to reduce recording ofbehavior other cess to dew and rain, along with soil water, for water up-
BEHAVIORAL OSMOREGULATION IN CRABS
422 C. A. COMBS ET AL.
HI
F *
5c5
normal
UJ
hem<'Concentrated
g
*
oIL
fw sw fw sw
g nornal
hemoconcentrated
O 40
fw sw fw sw
O
i
BEHAVIORAL OSMOREGULATION IN CRABS 423
mechanisms that enable B. lalro and G. lalandii to os- Harris, R. R., and G. A. Kormanik. 1981. Saltandwaterbalanceand
antennal gland function in three Pacific species ofterrestrial crab
moregulate behaviorally. (Gecarcoidealalamiii, Cardisomacarnifex. Birguslalro}. II.Theef-
fectsofdesiccation../ Exp. Zool. 218: 107-116.
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Dr. Robert Lishak, and John Newman for their contri- Hill,R.W.,andG.A.Wyse. 1989. AnimalPhysiology. 2nd.ed. Harper
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ScounptproirbtuetdinbgylaNbSoFratDoCryBsp8a8c-e01a9n2d6ftooraRdPvHic,ebayndfucnrdistifcirsomm. HKuogrgAmidanvn.si,kC,oA.mG.pK..A,.B,iaaonncddheKRm...ARP..hyHMsauironrlid.sa.3y:.192871119.-638.78Sa.lCtraunstdawcaetaenrmbeatlaabnocleiasnm.d
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