Ontogeny of Osmoregulation and Salinity Tolerance in Cancer irroratus; Elements of Comparison with C. borealis (Crustacea, Decapoda)

10 Pages·1991·3.8 MB·English

by  G Charmantier

Reference: Biol Bull 180: 125-134. (February,
Ontogeny of Osmoregulation and Salinity Tolerance in
Cancer Elements of Comparison with
irroratus;
C. borealis (Crustacea, Decapoda)
G. CHARMANTIER AND M. CHARMANTIER-DAURES
Laboratoire d'Ecop/iysiologie des Invertebres, Universitedes Sciences. Montpellier 2.
Place E. Bataillon. 3409? Montpellier tedex 05. France
Abstract. Osmoregulation and salinity tolerance were Hepalus ep/ie/iticiis. Lihinia cinarginata (Kalber, 1970),
studied in zoeae, megalopae, first crab stage (osmoregu- Sesaniui reticii/atnm (Foskett, 1977), Clibanarim vittatus
lation only), and adults ofCancerirroratus, and in zoeae (Young, 1979), CallianassaJamaica(Felderc/ a/., 1986),
and adults ofC. borealis. Alacrohrac/iiuni pelersi (Read, 1984), Uca snhcylindrica
In C. irroratus. salinitytolerancewasmoderatein zoeae, (RabalaisandCameron, 1985),Homarusamericanus, and
decreased inlatezoeae5,wasataminimum in megalopae. Penaeusjaponicm (Charmantier, 1986; Charmantier et
and increased in adults. The lower and upper lethal sa- a/.. 1984a, 1988).
linities for 50% ofthe animals (48 h LS 50) at 15C were For different reasons, including culture difficulties in
about 13-17%o/42-50%o in zoeae, 24%o/37%o in mega- late larval stages, Osmoregulation was frequently studied
lopae, and 8.5%o/65%o in adults. in larval stages only, particularly in brachyuran crabs.
In C. borealis. thecorrespondingvalues ofLS 50swere However, in the four latter species, Osmoregulation was
16-20%o/46-50%o in zoeae and 12%/65%o in adults. studied throughout the post-embryonic development in-
In both species, zoeae were hyper-osmoconformers; cludingpost-metamorphic stages, thusOsmoregulation in
adultswereisosmotic in highsalinitiesand slightly hyper- larvae, postlarvae, and adults could be compared. The
regulators in low salinities. In C. irroratus. the change ability to osmoregulate did not change along the devel-
from larval to adult type of regulation occurred from opment in somespecies. In otherspecies, metamorphosis
megalopa (hyper-osmoconformer) to first crab stage (hy- marked the appearance of the adult type of regulation;
per-regulator in dilute media), i.e.. after the completion among brachyurans, thiscase hasbeen so fardocumented
ofmetamorphosis. in only one species, U. snhcylindrica, the adults ofwhich
Osmoregulation and salinity tolerance appear corre- are strong hyper-hypo-regulators (Rabalais and Cameron,
lated and are modified at metamorphosis. These results 1985).
are discussed with an emphasis on the effects of meta- Consequently, one ofthe objectives ofthis study was
morphosis on Osmoregulation ofdeveloping decapods. to determine whether comparable changes in Osmoregu-
lation at metamorphosis exist in brachyurans with lower
Introduction abilitiestoosmoregulate, particularly in speciesofthege-
nus Cancer, which slightly hyper-regulate in lowsalinities.
While Osmoregulation has been extensively studied in Experiments designed to study the ontogeny ofOsmoreg-
adult crustaceans (review in Mantel and Farmer, 1983), ulation were performed on the most abundant Cancer
relatively few data are available on larval or post-larval species ofthe Canadian East coast, the rock crab Cancer
Osmoregulation, in the followingspecies: Rhilhropanopeus irroratusSay 1817. Comparative data were also obtained
harrisii (Kalber and Costlow, 1966), Cardisoma guan- from some developmental stages ofa sympatric species,
humi (Kalber and Costlow, 1968), Callinectes sapidus. the Jonah crab Cancer borealis Stimpson, 1859.
Numerous studies have dealt with the tolerance to sa-
Received 11 June 1990;accepted 27 November 1990. linity ofcrustacean larvae and postlarvae, but the corre-
125
126 G. CHARMANTIER AND M. CHARMANTIER-DAURES
lation between the salinity tolerance of different devel- vae, were modified forthecultureofcrab larvae. Seawater
opmental stagesand theircorresponding osmoregulatory was filtered to 50 ^m during the zoea development then
capabilities has only been experimentally investigated in suppressed; flow-rate was set at 2.5-3 1 min"' from zoeae
a few species, U. subcylindrica (Rabalais and Cameron. 1 to early megalops, then at 1.-1.5 1 min"1; a 280 ^m
1985), H. americann.s and P. japonicus (Charmantier et mesh screen wasused aroundthe overflow system. Water
al., 1988). temperature was set at 15C during the zoeal develop-
Thus, the second objective ofthis study was to deter- ment, then at 19C. Cephalothoracic length was about
mm mm mm
minethe salinity tolerance oflarval, postlarval, and adult 0.56 in zoeae 1, 1.5 in zoeae 5, 2.2 in mega-
CTW mm
stagesofC. irroratus(and, forthepurposeofcomparison, lopae, and was 2.3 in first crab stage (Char-
of C. borealis). and to attempt to correlate their osmo- mantier-DauresandCharmantier, 1991).Crablarvaewere
regulatory abilities and their salinity tolerance. This is of fed three times a day with live Anemia nauplii. Larvae
particular interest in Cancer species, the larvae ofwhich ofC. irroratuswereculturedtothesecondcrabstage, and
are submitted to different patterns ofsalinity changes: in those ofC. borealisto the third zoea. Aseach larval stage
C. irroratus, zoeae hatch offshore and, as development lastsseveraldays, moltingstageswere obtained according
proceeds, late larvae and postlarvae are found nearer to to the time elapsed from the preceeding molt, and three
shore (Sandifer, 1973). groupsofanimals, postmoltstage A. stageC,and premolt
In both species, theearly post-embryonicdevelopment stage D. were selected.
comprises one prezoea, five zoeal stages, one megalopal
stage, and several earlycrab stages(Sastry, 1977a, b). Fol- Preparatit>n <ifmedia
lowingawide acceptance, zoeae are larval stages, and the Experimental media were prepared in compartmented
following stages, beginning with the megalopa, are con- 250-1tanksforadultsand0.5-1plasticcontainersforlarvae
sidered postlarvae (Felder et al., 1985). and young crabs. Dilute media were prepared by adding
In C. irroratus, osmoregulation has been studied in tap water to seawater, and high salinity media were pre-
adultsandlargejuveniles(Thurbergrfal., 1973;Cantelmo pared by adding "Instant Ocean Synthetic Sea Salts"
etai. 1975;Neufeldand Pritchard, 1979),andpreliminary
(Aquarium Systems, Inc.) to seawater. All experiments
dataon osmoregulation arealsoavailable in theearlypost- were conducted at 15C. Salinities were expressed ac-
embryonic stages (Charmantier et al., 1989). cording to the osmotic pressure in mosm-kg ', and to
the salt content in the medium in %o. A value of3.4%o is
Materials and Methods
equivalent to 100 mosm-kg"1. Osmotic pressure was
Animals measured with an Advanced Instruments 31 LA orWes-
cor5000osmometer,andsalinityonaYSI 33salinometer.
Adult C. irroratus and C. borealis were caught by
SCUBA diving in summer and autumn in Passama-
Survival bioassays
quoddy Bay and transferred to the culture facility at the
Biological Station, St Andrews, New Brunswick, Canada. Due to the small numberofavailable animals, salinity
They were kept in tanks supplied with running seawater tolerance in adults was evaluated only from the number
(S^ 29-32%o;T s 12C)undernatural photoperiod, and ofsurvivingand dead animals in media ofdifferent salin-
were fed cod, squid, and shrimp (Pandalus borealis). In ities. Adultcrabswereprogressivelyadapted from seawater
September,twoweeksbeforetheexperiments, fourgroups todiluted orconcentrated media by adding freshwateror
ofcrabswere selected: large and small C. irroratus [ceph- Instant Ocean salts to the original medium; each change
mm
alothoracic width (CTW): 91 to 115 and 45 to 70 of 100 mosm-kg"1 in the salinity required about 24 h.
mm, respectively], and largeand small C. borealis(CTW: Between two changes ofsalinity, they were kept for two
80-110 mm and 57-71 mm). Males and females were days at constant salinity in each test medium, which dif-
equally represented in each group. They weretransferred fered from oneanotherbyincrementsof100 mosm kg"'
to 250-1 tanks with charcoal-nitrated recirculated seawater (=3.4%o).
kept at 15C. Only animals in molt stages C or Do (ac- Acute static 48-96 h bioassays were conducted with
cordingtothenomenclatureofDrach, 1939)wereretained zoeaeand megalopae held intest mediarangingfrom 100
for survival and osmoregulatory experiments. mosm kg"' toseawater(^900-1000mosm kg"')and to
Larvae of both species were obtained in spring and 1600 mosm-kg"1, and differing by increments of 100
summer from some ofthe aforementioned crabs. After mosm -kg '. Each bioassay was run on a group of 10
hatching, larvaewere transferred to40-1 planktonkreisels individuals and replicated. Animals were counted and
(Hughesetal., 1974)suppliedwith flow-through seawater dead animals removed at 0.5, 1, 3, 6, 12, 24, 36, 48, 72,
at a salinity of29-32%o under natural photoperiod. The 96 h according to the prescriptions ofSprague (1969) in
planktonkreisels, normally used for culturing lobster lar- toxicity studies. The criteria for death were total lack of
ONTOGENY OF CANCER OSMOREGULAT1ON 127
600 1000 1800 mosm.kg
20 30 40 60 n/
Medium
Figure 1. Salinity tolerance in adult Cancer irnatu,\ and C horciilis at 15C. Percent mortality of
animals according to the salinity ofthe medium. Number ofanimals at the start ofthe experiments in
seawater(SW): C' irnmiltis: 16(tolowsalinity media)and 8(tohigh salinity media); C borealis: 19and 7.
movement, immobility ofappendages and heart, and lack (=17% to 44%o). The LS 50 s were about 250 and 1900
ofresponse after repeated touches with a probe. Median mosm -kg"1 (s8.5 and 65%o). In adult C. borealis. no
lethal salinities (LS 50)and 95% confidence intervalswere mortality was observed between 600 and 1300
calculatedbytechniquesofprobitanalysis(Lichtfield and mosm -kg"1 (^20.4 and 44%o), and LS 50s were about
Wilcoxon, 1949; Finney, 1962)computerized on the Let- 350 and 1900 mosm -kg"' (12 and 65%o) (Fig. 1). No
curprogram (Zitko, 1982; Lieberman, 1983). LS 50swere difference in salinitytolerancewasdetected between large
calculated at 24, 48, and 96 h. Survival bioassays were and small crabs ofeither species.
not run in first and second crab stages due to the small In larvae and postlarvae ofC. irroratusthe 48 h LS 50
number ofavailable animals. in low salinity media varied around 450 60 mosm kg~'
(^15 2%o) in zoeal stages 1 to 4 and early 5, then in-
Osmoregulation creased from the end ofstage zoea 5 through early mega-
The hemolymph was collected from adult crabs via a lopae (^600 mosm -kg"1, 20%o) to a highly significant
hypodermic needle inserted through the articulation maximum value (correspondingtoa minimum tolerance)
membrane at the basis ofthe fourth or fifth pereiopods. of700 mosm kg"1 (=24%o) in intermolt megalopae. The
At least seven dayselapsed between hemolymph samples 24 h and 96 h LS 50s were, respectively, generally lower
were taken from the same animal. and higher than the 48 h value but followed the same
Zoeae, megalopae, and youngcrabs werequickly dried pattern ofvariation. Maximum LS 50s at 24, 48, and 96
on filterpaperand immersed in mineral oil toavoidevap- h occurred in megalopae with respective values of 520,
oration and desiccation. The hemolymph was then sam- 700, and 820 mosm -kg"1 (18, 24, and 28%o). differing
pled with a glass micropipette inserted in the heart. significantly from one another.
Osmotic pressure ofhemolymph was measured on an In high salinity media, the 48 h LS 50 ofC. irroratus
Advanced Instruments 31 LA orWescor 5000osmometer youngstagesvariedaround 1350 120mosm-kg"' (^46
(adults) or on a Kalber-Clifton micro-osmometer, with 4%o) in zoeal stages 1 to 5, then decreased in early meg-
reference to the osmotic pressure ofthe medium (young alopae (^1240 mosm kg"1, ^42%o)toa highly significant
stages). Student / tests were used for statistical compari- minimum valueof1 100mosm kg"1 (^37%o)in intermolt
sons. megalopae. The 24 h and 96 h LS 50s were respectively
higher and lower than the 48 h value; they followed the
Results same pattern ofvariation, decreasing to minima of 1 150
mosm-kg"1 (24 h: 39%o) and 1000 mosm -kg"1 (96 h:
Salinity tolerance
34%o) in megalopae (Fig. 2).
The ability of C. irroratus and C. borealis to tolerate In zoeae ofC. borealis. the 48 h LS 50 varied around
low and high salinities varied with post-embryonic de- 530 60 mosm -kg"1 (^18 2%) in low salinities. The
velopment. 24 h and 96 h LS 50s were markedly lower and higher
Adults of C. irroratus survived without mortality in than the 48 h LS 50. The differences between 96 h and
media ranging from 500 mosm kg"' to 1300 mosm kg"' 24 h LS 50s were more important than in C. irroratus: in
128 G. CHARMANTIER AND M. CHARMANTIER-DAURES
700 6
300
A C DA C DA C DA C DA C DA C Moltstages
1 Zl - ' Z2 ' Z3 Z4- -Z5- -Mgl L.stages
Days
Figure 2. Salinity tolerance inzoeae 1-5 and megalopaeofCancerirrorulti.iat 15C. Variationsin LS
50in %oand mosm kg"' accordingtolarvaland molt stagesand todaysofdevelopment, in highand low
salinities(upperandlowertraces). Eachpointrepresentsthemeanvalueofatleasttwodeterminationsfrom
10 animals, with 95% confidence interval. Closed triangles: 24 h LS 50. Closed circles: 48 h LS 50; open
circles: 96 h LS 50.
some instances (early zoea 1 and zoea 2), the 24 LS 50 to a dilute medium of 500 mosm -kg ' (17%o), the he-
wasabout 300mosm kg"' (10%o),the96 h LS50reaching molymph osmotic pressure stabilized within 1 to 2 h in
about 740 mosm kg ' (25%). In high salinities, the48 h zoeae 1 and 5. In adults transferred from seawater to a
LS 50variedaround 1420 60 mosm kg"' (^48 2%o); dilute medium of 677 mosm-kg"' (23%o), the corre-
24 h and 96 h LS 50s were respectively higher and lower sponding time was 24 h (Fig. 4). The time of osmotic
(Fig. 3). adaptation toconcentrated mediawas nottested; in other
species, it wasshorterthan thetimeofadaptation todilute
media (Charmantier ct ai. 1988). In all subsequent ex-
Osmoregulation
periments and in both species, we kept the young stages
Adaptation time. The time of adaptation after a 6-24 h and the adults 3-4 days in each medium before
change in the environmental salinity was evaluated in sampling.
stage C zoeae 1 and 5 and in adults ofC. irroratus. After Osmoregulation. Adults of C. irroratus and C. bo-
a rapid transfer from seawater at 920 mosm kg"1 (31%o) realiswere almost osmoconformers in high salinitiesand
ONTOGENY OF CANCKR OSMOREGULATION 129
regulationindilutemediawasslightlymorehyper-osmotic
in premolt (zoeae 1,4 at 500 mosm kg"': P < 0.05) and
less hyper-osmotic in post-molt (zoeae 2, 3, 4 at 500 and
900 mosm kg"': P < 0.01). Megalopae were also hyper-
osmoconformers. The pattern ofosmoregulation seemed
to change after the completion of metamorphosis. First
crab stageswerealmost osmoconformers in seawaterand
theirregulation wasslightly hyper-osmotic inadiluteme-
diumof500mosm kg '. 11% (hemolymph-medium dif-
ference of55 16 mosm-kg"') (Fig. 6).
Zoeae 1 to 3 of C. borealis had the same pattern of
hyperosmoconforming regulation aszoeaeofC. irroratus
(Fig. 7).
Discussion
Sa/initv tolerance
700 ~
O
In Cancer uroraliis, the interval oftolerable salinities
6
tends to decrease at the end of the larval development
and is minimum in megalopae. At thisstage, the 96 h LS
50sareabout28%oand 34%o,which meansthat megalopae
are almost restricted to seawater. In adults, approximate
48 h LS 50s are 8.5%o and 65%o. The wide euryhalinity
demonstrated by adults could be partly related to the rel-
atively short time ofexposure to the different media and
totheprogressiveadaptation tochangingsalinities. Long-
term exposure to extreme salinities could yield more re-
DA C C Molt stages strictive results.
-zi -22- Lstages These resultsare in agreement with previousdata. Sas-
20 25 Days try (1970) found that at 15C, only 5.5% of megalopae
Figure3. Salinitytoleranceinzoeae [-3ofCancerborealisat 15C. ofC. irroratus molted to the first crab stage in a medium
Variationsin LS50in % andmosm kg"' accordingtolarvaland molt of 15%o, while this molt was successful in a higher per-
stagesandtodaysofdevelopment, inhighandlowsalinities(upperand centage ofmegalopae in media ranging from 20 to 35%o,
lforwoemrt1r0acaesn)i.maElasc,hwpiotihnt9r5e%precsoennftisdtehnecemeiantnervvaallu.eColfotswedodtertiaenrgmliens:at2i4onsh withamaximum rate of76% in amedium of30%o. Com-
LS 50;closedcircles: 48 h LS 50;opencircles: 96 h LS 50. plete development from zoea 1 to first crab stage was
found possible at 15C between 20 and 35%o (Sastry and
McCarthy, 1973) or 25 and 35%o, but survival exceeded
seawater, and their regulation was slightly hyper-osmotic 50% onlyin 30-35%. (Johns, 1981). In adults, McCluskey
in dilute media(Fig. 5). Nodifference ofhyper-regulation (1975,cited in Bigford, 1979) found survival waspossible
wasdetectedbetween largeand small adultsin C. bomilis. for three days at 5-8C in salinities ranging from 10 to
In C. irroratus large crabs were significantly stronger reg- 20%o (the upper limit was not tested).
ulatorsthan small crabs(hemolymph-medium differences Compared to the larvae of C. irroratus, zoeae of C.
of71 7 and 55 13 mosm kg"1 respectively, P< 0.005, borealis were less tolerant to prolonged exposure to low
in a 500 mosm kg"1; 17%o, medium). The ability to hy- salinities. In C. borealis, Sastry and McCarthy (1973)
per-regulate in dilute media wassignificantly higherin C. foundthat complete larval development wasonly possible
irroratusthan in C. borealis (in large crabs, hemolymph- ina medium of30% at 20C. Theseandourresultsdem-
medium differences of71 7 and 37 5 mosm-kg ', P onstrate that C. borealis is more stenohaline than C ir-
< 0.001, in a 500 mosm -kg"1, 17%o, medium). roratus, and, in particular, less tolerant to low salinities
Zoeae 1 to 5 ofC. irroratus in molting stage C hyper- during the larval development and in adults.
osmoconformed at almost all tested salinities, i.e., their
hemolymph osmotic pressure varied as a function ofex- Adaptation time
ternal osmotic pressure but remained above external by
about 15-50 mosm kg"1;atthelowesttestedsalinity(300 In C. irroratus. the time ofosmotic equilibration in a
mosm kg"1), zoeaewere isosmotic. In somezoeal stages. dilute medium is about 1 to 2 h in larvae and 24 h in
130 G. CHARMANTIER AND M. CHARMANTIER-DAURES
Q.
E
Figure4. Changein hemolymphosmoticpressureinstageszoeae 1 and5ofCancerirroratusafterrapid
transferfrom seawater(920 mosm kg"', 31%)toadilute medium (500 mosm kg"', 17%o), and in adults
ofC. irroratusafter rapid transfer from seawaterto677 mosm kg~', 23%o. at 15C. Each point represents
the mean valueofdeterminations from 3 to 5 zoeaeor 5 adults, with 95% confidence interval.
adults. Adaptation time is thus size-dependent, which (Jones, 1941; Engelhardt and Dehnel, 1973; Hunter and
could be related to differences in the volumes of water Rudy. 1975).
and ion exchanges and to differences in tegument per- Zoeae ofC. irroratus hyper-osmoconform in all tested
meability between development stages. These times of salinities. Most decapod larvae that have been studied
adaptation are similartothose ofthecorresponding stages
ofother species (see Charmantier el ai, 1988).
Osmoregulation
In C. irroratusand C. borealis, adultsosmoconform in
high salinitiesand seawaterand slightly hyper-regulate in
dilute media. The ability to hyper-regulate is higherin C.
irroratus.
Asimilarpattern ofosmoregulation hasbeendescribed
in C. irroratusand otherspeciesofCancer, buttheability
to hyper-regulate varies with the species, although other
factors such as size and temperature can affect this pa-
rameter. In media of approximately 500 mosm-kg"',
17%o, at temperatures of =15-20C, the difference be-
tween the osmotic pressures ofhemolymph and medium Medium (mosm.kg )
expressed in mosm-kg"' is about 15 in C. antennarius Figure5. Variationsinthedifferencebetweentheosmoticpressures
(Jones, 1941), 30-40 in C borealis (this study), 50 in C. ofhemolymph and medium according to the osmotic pressure ofthe
pagurus (Wanson et ai, 1983), 50-120 in C. irroratus mIe5dCi.uEmacinhlpaorgientanrdepsrmeaselnltasdtuhletsmoefaCnanvcaelrueirorfordaeltuesraminndatC.iobnosrefarloisma7t
(Thurberg et al.. 1973; Cantelmo et ai, 1975; Neufeld to 10animals(exception inlowestsalinity:4-6animals)with95%con-
and Pritchard, 1979; this study), 150-250 in C. nwgister fidence interval.
ONTOGENY OF CANCER OSMOREGULATION 131
60
80
20
40
20 Zl
^ 40
E
1 20
E 60
40
T) -c
a.
20
Z2
I I 20
40 . Cl
20 20
I o L
300 500 700 900 1100 1300 300 500 700 900 1100 1300
Medium (moim.kg-1) Medium (mosm.kg-1)
Figure6. Variationsinthedifferencebetweentheosmoticpressuresofhemolymphandmediumaccording
totheosmotic pressureol the medium in zoeae 1-5, megalopae. and firstcrabstageofCancerirroratiisat
15C. Eachpointrepresentsthemeanvalueofdeterminationsfrom9-15animals(5-10animalsinextreme
salinities)with 95%confidence interval. O O: post-molt; : stageC; A-- A: premolt.
hyper-osmoconform in salinities that they normally en- regulate, evaluated by thedifference between the osmotic
counter in their environment (Charmantier ct ui, 1988). pressuresofhemolymph and medium inadilute medium,
Thiscouldbeconsideredanadaptation ofsmallorganisms increases with size in adults: in a medium of 500
toplanktonic or pelagic life. The slight positivedifference mosm-kg"1, 17%, this difference was 55 16
in osmotic pressure between hemolymph and medium mosm-kg"' in first crab stage, 55 13 mosm-kg"1 in
maintainsan osmotic influx ofwater, which in turn favors small adults, and 71 7 mosm-kg"1 in large adults. As
the turgescence of the body and particularly of the ex- in C. irroratiis, zoeae ofC. borealishyper-osmoconform,
tended appendages and exopodites involved in the buoy- while adults have a slight hyper-isoregulation. In a pre-
ancy ofthe larvae. In a few zoeal stages of C. irroratiis, liminary study. Brown and Terwilliger (1989) found that
the osmotic pressure of hemolymph is affected by the megalopae and first crabs ofC. magisterwere weaker os-
molting stage, increasing in premolt and decreasing in moregulatorsthanadults, after8 hexposuretodilute me-
postmolt but much less regularly than in other species dia. A comparison with our results is difficult due to the
like Rhithropanopeus harrisii(Kalberand Costlow, 1966), lack of numerical data. Additionally, it is possible that
Cardisomagiianhumi(KalberandCostlow, 1968), Hom- the short time of exposure did not allow for complete
arus americanus and Penaeusjaponicus (Charmantier ct osmotic equilibration in adults.
a/.. 1988). Like zoeae, megalopae ofC. irroratiis hyper- In a recent study, we reviewed the evolution of os-
osmoconform in all media. Firstcrabstagesosmoconform moregulatory abilities that have been described for
in seawater, but they hyper-regulate in a dilute medium. the post-embryonic development ofdecapod crustaceans
Thus, the adult type of osmoregulation seems to be ac- (Charmantierel ai. 1988). Mostdecapod larvae that have
quiredatthefirstcrabstage. However,theabilitytohyper- been studied, including zoeae ofC. irroratiis and C. bo-
132 G. CHARMANTIER AND M. CHARMANTIER-DAURES
latory capacity ofearly post-metamorphic stages. Forex-
60
ample, in Sesarmu reticulatum studied by Foskett, 1977,
zoeae and megalopae were hyper-osmoconformers and
adults were hyper-hyporegulators, but early crab stages
were notstudied. Foskett stated: ". . . evenby late mega-
lopstheadultosmoregulatory responseisstill notattained.
Examination of osmoregulation in early juvenile crab
stages may reveal osmoregulatory responsesthataretran-
o>
J* sitional between the larval and adult forms."
E
o The few studies that were conducted in decapods
throughout the post-embryonic development, including
ED post-metamorphic stages, confirm this statement. The
O transition from larval toadulttypeofosmoregulation may
occur rapidly when metamorphosis itselfis sudden, as in
a //. americanus, or may be progressive when metamor-
phosis is spread over several post-larval stages as in P.
japonicus (Charmantier et al.. 1988). There is a lack of
agreement on the exact timing of metamorphosis in
brachyurans: it has been located either at the molt from
Z3 megalopa to first crab stage (Costlow. 1968), or at the
molt from last zoea to megalopa (Felder et al.. 1985).
Actually, most morphological changes result from the
300 500 700 900 1100 1300 molt separating the last zoea and the megalopa and, in
Medium(mosm.kg"1) U. subcylindrica, thetypeofosmoregulation alsochanges
Figure7. Variationsinthedifferencebetweentheosmoticpressures atthismolt(RabalaisandCameron, 1985). However,this
ofhemolymph and medium according to the osmotic pressure ofthe physiological modification occursonlyafterthe moltsep-
medium inzoeae 1-3ofCancerborealisat I5C. Each pointrepresents aratingthe megalopaandthe firstcrabstagein C. irroratus
tinhteermveala.nOvalueOo:fdpeotsetr-mmoilnta;tionsfrom:1s0taagneimCa;lsAw-it-hA9:5p%recmoonlfti.dence (Atdhdiistsitoundayl)l,ya,nadspsotsastiebdlbyyinFe5l.dreerteitcuall.a.t(u1m9(8F5o)s,ke"titn,a1l9m7o7s)t.
all the Decapoda, some ontogenic changes in locomotion,
realis, are hyper-osmoconformers or weak regulators, an feeding, and habitat coincide with early postlarval
exception being the larvae of Macrobrachium petersi growth." Thus, in ouropinion, metamorphosis in brach-
(Read, 1984),which areconfronted with very lowsalinities yurans requirestwo moltstobecompleted and the mega-
in their natural environment and which can efficiently lopa, while clearly postlarval, is a transitional stage be-
regulate the osmotic concentration oftheir hemolymph. tween the larvae and the postmetamorphic stagesstarting
During or after the larval phase, different patterns ofon- with the first crab stage.
togeny ofosmoregulation have been described, which we In summary, studies conducted on the species ofthe
proposed to separate into three groups (Charmantier et thirdgroup ofdecapodscited abovedemonstrate that the
al., 1988). In onegroup ofspecies, osmoregulation varies completion ofmetamorphosis yieldsa change tothe adult
littlewith developmental stage; theadultsofthese species type ofosmoregulation. We propose the hypothesis that,
are often weak regulators or osmoconformers, like He- in mostspeciesinwhichlarvaearehyper-osmoconformers
patusepheliticusand Libinia emarginuta (Kalber, 1970). orweak regulatorsand adultsareefficientosmoregulators,
InM.petersi(Read, 1984),which livesin variablesalinities the transition from the larval type to the adult type of
dueto its migration, the adult type ofregulation isestab- osmoregulation occursat metamorphosis. Moregenerally,
lished asearly as the first larval stage. In a third group of metamorphosiscan beconsideredacombination ofmor-
species, which includes Uca subcylindrica (Rabalais and phological, ecological, behavioral, and physiological
Cameron, 1985), Homarus americanus, Penaeusjapon- changes (Costlow, 1968; Charmantier et al.. I984b).
icus(Charmantieretat., \988), and Cancerirroratus(this
study), metamorphosis markstheappearanceoftheadult Relation between osmoregulation andsalinitytolerance
type ofregulation. In other species that do not still fit in
those three categories, in which "no clear trend toward In C. irroratus and C. borealis. zoeae are weak regu-
development ofadult osmoregulatory patterns toward the lators and their salinity tolerance is comparatively mod-
end oflarval life" was found (Foskett, 1977), this could erate or low. In megalopae ofC. irroratus, salinity toler-
be due to the lack of information about the osmoregu- ance is minimum just before the pattern ofosmoregula-
ONTOGENY OF CANCER OSMOREGULATION 133
tion changes. Under natural conditions, developing Charmantier, G., M. Charmantier-Daures, N. Bouaricha, P. Ihurt.
brachyurans are known to settle on the bottom during J.-P.Trilles, and D. K. Aiken. 1989. Ontogeny ofosmoregulation
the megalopal stage, usually near the shores (Sandifer, and salinity tolerance in Homarus americanus, Penaeus laponicus
1973), i.e.. in an environment subjected to possible vari- CharamnadntCiaenrc-eDrauirrersor,atMu.s,Aamn.dG/.<><C>/h.a2r9m:an1t5i5eAr.. 1991. Mass-cultureof
ations ofsalinity. The limited salinity tolerance ofmega- Cancerirroraluslarvae(Crustacea, Decapoda):adaptationofaflow-
lopaecouldcause high ratesofmortality, which havebeen through sea watersystem. Aquaculture.
noted indifferent speciesofCancer, at least underculture Costlow, J. D., Jr. 1968. Metamorphosis in crustaceans. Pp. 3-41 in
cUonnsdufiftiicoinesn(tChnaurmmbaentrieorf-aDvaauirleasblaendanCihmaarlmsanptrieevre,nt1e9d91u).s DracMChreo,tfatPms..o1rN9p3eh9ow.siYsoM.rukW.e.etEtckyicnleadn'dinLt.erI.muGielbcehretz,leedssC.ruAsptpalceetsonD-eCceanptoudreys-.
from determining the salinity tolerance of early crab Ann lust Oceanogr.. Monaco \9: 103-341.
stages, in which the pattern of osmoregulation has Engelhardt, F. R., and P. A. Dehnel. 1973. Ionic regulation in the
changed. We may suppose that their salinity tolerance Pacificediblecrab. Cancermagister(Dana). Can. J 7.ool. 51: 735-
has correlatively increased. In adults ofboth species, the 743.
ability to osmoregulate is higher and so are their salinity Feldmeorr.eJg.ulMa.t,ioDn.iLn.thFeeledsetru,arainndeSg.hoCs.tHsahnridm.p1C9a8l6.lumaOsnstaogieanmayicoefn.oss-e
tolerances. Compared to C. borealis, adult C. irroratm var. louisianensis Schmitt (Decapoda. Thalassinidea). J Exp. Mar
arestrongerhyper-regulators in dilute mediaandare more Biol Ecol. 99:91-105.
toleranttolowsalinity. Thus, aspreviously noted in Mac- Felder, D. L., J. \V. Martin, and J. \V. Goy. 1985. Patterns in early
robrachiwnpetersi (Read, 1984), Uca subcylindriai (Ra- postlarvaldevelopmentofdecapods. Pp. 163-225 inLarvalGrowth,
balais and Cameron, 1985), Homarus americanus and A. M. Wenner, ed. A. A. Balkema. Rotterdam. Boston.
Penaeusjaponicus (Charmantier et til., 1988), there is a FinnSeiyg,moDi.dJ.Res19p6o2n.se CPruorbviet ASneacloynsdisEdi1tiSotna.tiCstaimcbalriTdrgeeatUmneinvt. oPfretssh,e
strongcorrelation between increased ability toosmoregu- London.
late and improved salinity tolerance. Foskett, J. K. 1977. Osmoregulation in the larvae and adults ofthe
grapsidcrabSesarma rclicutalum Say. Biol Bull 153: 505-526.
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Partofthisstudywassupported byagrant from NATO. 36: 129-132.
We thank Dr. D. E. Aiken for providing lab space and Huntienr,thKe.DCu.,ngaenndePs.sPc.raRbu.dyCaJnr.ce1r97m5a.gisOlsemrotDiacnaa.ndCoiomnipcrBeiguolcahteiomn
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