The Effect of Environmental Factors on Development of the Land-Grab, Cardisoma guanhumi Latreille

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1 AM. ZOOLOGST, 8: (68). The Effect of Environmental Factors on Development of the Land-Grab, Cardisoma guanhumi Latreille JOHN D. COSTLOW, JR., AND CAZLYN G. BOOKHOUT Duke University Marine Laboratory, Beaufort, N. C , and Department of Zoology, Duke University, Durham, N. C. SYNOPSS. Larvae of the land-crab, Cardisoma guanhumi, Latreille. were maintained in 24 different combinations of salinity and temperature from the time of hatching. Survival to the first crab occurred in salinities of -45 p.p.t., 25 and 30 C. Duration of the five zoeal and one megalops stages was similar in salinities of -40 p.p.t., but at and 45 p.p.t. a greater period of time was required f6r total development. Mortality of.all the larvae at C suggests that temperature plays a more important role in survival and distribution of the larvae of C. guanhumi than salinity. ncrements of size in crabs during the first seven post-larval molts were similar in salinities of 5-35 p.p.t., 25 C, but in fresh water increase in size at the time of molting was reduced. Although there was no apparent relationship between frequency of molting and salinities of 5-35 p.p.t., the duration of intermolt was reduced in crabs maintained in fresh water, and survival was also lower. From the present study there is no indication that the morphological and physiological processes that are associated with adaptation of the adult crab to the terrestrial environment are initiated during larval development. Although the adult crabs have successfully penetrated the terrestrial environment, the pelagic larvae are still subject to the numerous ecological variables of the estuarine and marine environments. The varying degrees of adaptation of marine crabs to the terrestrial environment have been the subject of a number of studies within recent years. These have included investigations of morphology (Bliss, 63), growth (Herreid, 67), ecology (deoliviera, 46; Gifford, 63), and physiology (Bliss, Wang, and Martinez, 66; Gifford and Johnson, 62; Gross, 55, 63, 64). These studies have dealt largely with adult crabs, which retain their link with the marine environment through pelagic larval stages. There are relatively few observations on the embryonic and larval phases of development of semi-terrestrial and terrestrial decapods. Moreira (13) gave a general description of the embryology and first stage zoea of the land-crab, Cardisoma guanhumi, and Cabrera (65) described These studies were supported by a grant (GB 5711) from the National Science Foundation. The authors wish to express their appreciation to Miss Berta Willis and Mrs. J. Herring for their technical assistance throughout the study. We are also indebted to the Second Marine Air Wing, Cherry Point, North Carolina, for their assistance in transporting the live crabs from Puerto Rico to Beaufort. 399 the first larva of another terrestrial crab, Gecarcinus lateralis. Costlow and Bookhout (67) reared the larvae of C. guanhumi from hatching through metamorphosis in the laboratory and described five zoeae and one megalops. Although there are isolated references to the tolerance of eggs and first stage zoeae of several species of land-crabs (Gifford, 63; Cannon, 23), nothing is known of the effect of environmental factors on larval development and distribution, the extent to which adaptation by the adult may be reflected in the larval stages, or when the morphological and physiological changes associated with adaptation to the terrestrial environment may occur in the process of development. n the present study Cardisoma guanhumi Latreille was reared from hatching to the seventh post-larval stage under controlled conditions in the laboratory. The major objectives of the investigation were: (1) to determine the effect of temperature and salinity on length of larval life and survival through metamorphosis to the first crab; (2) to study the effect of salinity on early post-larval 1 molting frel n this study the molt from megalopa to the on 26 November

2 400 JOHN D. COSTLOW, JK., AND CAZLN G. BOOKHOUT first crab is considered metamorphosis. Stages prior to metamorphosis are designated as larval, and postlarval refers to the first and subsequent crab stages. quency and size increments; and (3) to determine if the processes that are associated with adaptation of the adult crabs to the terrestrial environment begin during larval development, at the time of metamorphosis, or during the period of early post-larval development. > S m3 «qqq^j o oi ij* d to otj PROCEDURES Ovigerous females were collected and sent by air from Puerto Rico to the Duke University Marine Laboratory, Beaufort, N. C, where the larvae were hatched at 25 C, 25, 30, and 35 p.p.t. by removing the eggs and maintaining them in compartmented boxes on an Eberbach variablespeed shaker (Costlow and Bookhout, 60). At the time of hatching, the zoeae from 25 p.p.t. were transferred gradually to the lower salinities and those from 35 p.p.t. to the higher salinities. Although the temperature of the water to which the zoeae were transferred was 25 C, it was gradually lowered to C or raised to 30 C. Each day the larvae were transferred to filtered sea-water of the same salinity and temperature and freshly hatched Artemia nauplii were added. At this time the mortality of larvae within each series was recorded. At the time of the final zoeal molt to the megalops stage, the larvae were segregated into plastic compartmented boxes in order to determine the time required to complete metamorphosis to the first crab. At the time of metamorphosis the first crabs were transferred to glass fingerbowls and immersed in fresh water or salinities of 5,, 25 and 35 p.p.t. seawater maintained at 25 C. They were changed every second day to filtered water of the same salinity and temperature and fed Artemia nauplii. The time of the first seven postlarval molts was recorded for each of the crabs in the five experimental series, and the exuviae were measured, initially with a micrometer mounted in the ocular of a.5 So d E 3 OOOODOOOOHO on 26 November

3 ENRONMENTAL EFFECTS ON CRAB LARAE 401 Survival of Cardiso/na guanlwmi larvae era/? _ndanfl _Q DUD mecplopclbo crab hatch to megalopa. to ft 10"ft 25^0^)40 4 FtC. 1. Zoeal, megalops, and total survival o Cardisoma gunnhumi larvae maintained at 24 different combinations of salinity and temperature. dissecting microscope and later with a vernier caliper. RESULTS The combinations of salinity and temperature used, the original number of zoeae in each combination, the number that reached the megalops stage, and the number of larvae that metamorphosed to the first crab are shown in Table 1. At C, less than 10% of the zoeae completed the molt to the megalops in salinities of p.p.t. and none of these survived to metamorphosis to the first crab (Fig. 1). At 25 C, survival to the first crab varied from 10-26% in salinities of -40 p.p.t. (Fig. 1). At 10 p.p.t., however, the larvae did not develop beyond the second zoeal stage and at 45 p.p.t., only 0.5% completed development. At 30 C, survival was similar to that observed at 25 C although the percentage of survival *at p.p.t. was higher at 30 C. A small on 26 November

4 402 JOHN D. COSTLOW, JR., AND CAZLYN G. BOOKHOUT Length of Lvrval U Ccuxlisoma guanjuwu hatch ho crab 40 C j 40 M: megalopaho crab n o 60 to mecfalopa 'C n n n n i i i i n r P T ^ FG. 2. Duration o zoeal stages, raegalops, and- Cardisoma guanhumi maintained at 24 different entire period of development for larvae of combinations of salinity and temperature. on 26 November

5 ENRONMENTAL EFFECTS ON CRAB LARAE 403 Size ncrements in C&rdisoma guanfwmi Post/arval Molts FG. 3. Size increments for juvenile Cardisoma guanhumi maintained in fresh water and four salinities during the first seven post-larval molts. percentage of the larvae survived to metamorphosis at and 45 p.p.t., 30 C, but none of the larvae completed development at 10 p.p.t. Survival after the larvae reached the megalops stage was consistently higher than survival during zoeal development at both 25 and 30 C. As shown in Figure 2, development of the five zoeal stages required a period approximately twice as long at C as at 30 C. For example, at 30 p.p.t., C, the time from hatching to the megalops varied from days while comparable development at 30 C required days. The minimum time required for development of the megalops to the first crab was on 26 November

6 404 JOHN D. COSTLOW, JR., AND CAZLYN G. BOOKHOUT TABLE 2. Size increments. Molt No. of crabs Mean width, mm nitial Final Average increase % increase S.D.± S.E. Fresh water 25 C 5%. 25 C %, 25 C %, 25 C 35%,, 25 C similar at 25 and 30 C, but the mean and maximum periods for development from hatching to the first crab were longer at 25 C. Duration of the larval stages was affected only by extreme salinities (Fig. 2). At 25 C there was more uniformity in the time required for complete development in salinities of -45 p.p.t., with the mean times for larvae in these seven salinities varying by 11 days. At 30 C, there was uniformity in duration of development to the first crab stage in salinities of -40 p.p.t., but the mean times for complete development varied by days at and 45 p.p.t. As shown in Figure 3, increase in size of the crabs through the first seven postlarval molts was similar in salinities of 5-35 p.p.t., 25 C, but in fresh water, size increments of the crabs were reduced. The variation in size increments is shown for crabs of all experimental series in Table 2. Although the size increments for crabs maintained in fresh water were reduced, the molting frequency was accelerated as shown in Figure 4. The first four postlarval molts were completed within 31 days by the crabs maintained in fresh water, while these same molts required 51 days in 35 p.p.t. Although this acceleration persists through the time of the seventh molt in crabs maintained in fresh water, there was not an obvious relationship between duration of intermolt period and salinity in crabs maintained in the other experimental salinities. The variations in on 26 November

7 ENRONMENTAL EFFECTS ON CRAB LARAE 405 molting frequency are shown for crabs of all experimental salinities in Table 3. As shown in Table 4, crabs maintained in fresh water had the lowest percentage survival, with the highest mortality after the fourth post-larval molt. n the other salinities there was little mortality during this same period and the gradual decline Pest larval ntermoitduration Card&orm guaritwmi Salinity ppt FG. 4. Duration of intermolt periods for juvenile Cardisoma guanhumi maintained in fresh water and four salinities during the first seven post-larval molts. on 26 November

8 406 JOHN D. COSTLOW, JR., AND CAZLYN G. BOOKHOUT Molt Fresh water, 1 5% e, 25 "C &,, 25 C 1 25% c, 25 C 35%,,, 25 C TABLE 3. Molt Mean 25 C S.D.± frequency-days S.E N in numbers of crabs in all series would suggest that mortality was associated with some factor other than salinity. DSCUSSON n considering the general ecology of adult C. guanhumi, Gifford (63) points out that crabs of this genus are circumequatorial, with a range which includes the east coast of America from Florida to Brazil, as well as the Caribbean slands. Although most of the previous studies on C. guanhumi have dealt with crabs from Florida, the northern limit of this species, the crabs are numerous in parts of Puerto Rico and subject to the same general influences of salinity and temperature. Throughout its range, C. guanhumi is rarely found more than 8 km from the sea. Under natural conditions, however, the adults spend much of their time in burrows, which extend to ground water. Although the adults can live for extended periods in moist air, they will not survive more than two days under conditions of severe desiccation (GifFord, 63). nformation on the larval development of crabs of the genus Cardisoma is limited largely to observations associated with other studies on the adult animals. Cannon (23) attempted to rear the larvae of the West African species, C. arm a turn, by removing the eggs from the female and maintaining them in artificial sea-water, tap-water, and a mixture of equal parts of sea-water and tap-water. The eggs in tap-water did not survive but those in the other two salinities did hatch. From Cannon's figures it must be assumed that the larvae hatched at "prezoeal" rather than the normal first zoeal stage (23). None of the larvae lived beyond a few days, and observations on the later zoeal stages or megalops of this species are not available. Gifford (63) found that although a small number of eggs would hatch as "pre-zoea" in TABLE 4. Survival of C. guanhumi at 25 C during first six post-larval molts. Fresh water 5p.p.t. p.p.t. 25 p.p.t. 35 p.p.t. Molt No. % No. % No. % No. of /o No. % on 26 November

9 ENRONMENTAL EFFECTS ON CRAB LARAE 407 drainage ditch water, the larvae did not live. Hatching and survival of the larvae increased as the salinity was increased to 50% of natural sea-water. n salinities above 50%, however, hatching was reduced. Although none of the larvae survived beyond the first molt, Gifford (63) observed longer periods of survival of first stage zoeae in salinities of 80-90% sea-water. n the present study, although comparative figures on hatching in different salinities are not available, the larvae did hatch and survive in salinities of p.p.t. (ca % sea-water). The effect of environmental factors on survival of those estuarine and marine crabs that have been successfully reared in experimental conditions of the laboratory has shown considerable variation between species. Larvae of some crabs, such as Rhithropanopeus harrisii, will develop over a wide range of salinity ( p.p.t.) and temperature ( -30 C) (Costlow, Bookhout, and Monroe, 66). Larvae of other species, Sesarma cinereum and Panopeus herbstii, will complete development in a more narrow range of salinity and temperature (Costlow, Bookhout, and Monroe, 960, 62). The larvae of still other species, primarily those that are confined as adults to oceanic waters (Hepatus ephililicus) will complete metamorphosis successfully only in a narrow range of higher salinities (Costlow and Bookhout, 62). n experiments with larvae of a number of these species it has been demonstrated that survival is not affected solely by one environmental factor but rather by combinations of salinity and temperature. n the present study, survival of the larvae of C. guanhumi through metamorphosis occurred in salinities of -45 p.p.t. (ca % sea-water) at 25 and 30 C, although the per cent survival at and 45 p.p.t. was extremely low. At C, only a few larvae reached the megalops stage and only in salinities of p.p.t., and these did not survive to metamorphosis. The absence of any survival at C would suggest that temperature is a more important ecological factor than salinity in the larval development of C. guanhumi, as well as in its distribution. The length of larval life of some species of estuarine crabs is also known to be affected by environmental factors. Development of larvae of S. cinereum required a longer period of time in low salinities than in higher salinities (Costlow, Bookout, and Monroe, 60) and the duration of the megalops stage of Callinectes sapidus has been shown to be prolonged as salinities increased from to 40 p.p.t., although this effect was coupled with low temperatures (Costlow, 67). Development of the four zoeal stages and one megalops of another estuarine crab, Rhithropanopeus harrisii, was, however, unaffected by salinities of 5-35 p.p.t. and only slightly longer in salinities of 2.5 and 40 p.p.t. The length of larval development of crabs that are normally confined to the marine environment, however, has generally not shown any tendency to be affected by salinity. The larvae of Hepatus epheliticus (Costlow and Bookhout, 62), Ovalipes ocellatus (Costlow and Bookhout, 66), and Cyclograpsus cinereus (Costlow and Fagetti, 67) required the same amount of time for development in the limited range of experimental salinities that would permit complete larval development and metamorphosis. There was little evidence of effects of salinity on the duration of the zoeal stages of C. guanhumi. At 25 C, in salinities of -45 p.p.t., the mean time for development of the megalops to the crab varied by 7 days but there was not a consistent trend associated with increased or decreased salinity (Fig. 2). At 30 C, in salinities of -35 p.p.t., this variation did not exceed one day but, as the salinity increased to 40 and 45 p.p.t., the variation in mean time of magalops duration increased to 14 days. As with most other species which have been reared in the laboratory, development proceeds faster at 30 C than at either 25 or C but the mortality of all larvae at C prevents any direct comparisons of the time re- on 26 November

10 408 JOHN D. COSTLOW, JR., AND CAZLYN G. BOOKHOUT quired for total development at and 30 C. Tolerance of the eggs and larvae of C. guanhumi to a relatively wide range of salinity, while suggesting adaptation to the estuarine and marine environments that are normally adjacent to the populations of adults of this species, does not indicate any greater adaptative value to terrestrial than to other environments. The spawning period of C. guanhumi extends from June to December and the majority of the ovigerous crabs migrate to "salt-water" at the time of the full moon, completing the journey in one or two nights (Gifford, 63). The egg masses of females that Gifford captured, and thus prevented from spawning, disintegrated rapidly. n the natural environment, a number of factors could contribute to such a delay in reaching optimum conditions for spawning, and the survival of eggs and larvae in waters of lower salinity would permit the female to spawn at the time of maximum development of the eggs rather than lose the several hundred thousand eggs which are hatched at each spawning. Those larvae that were hatched in the higher salinities of oceanic waters would also survive and the normal development and metamorphosis that has been observed in a wide range of salinities would result in greater survival than recorded for larvae of oceanic species with a relatively narrow range of salinity tolerance. The survival of the megalops stage in salinities of -45 p.p.t., higher than that observed for the five zoeal stages, may be an adaptation to the estuarine conditions which this stage encounters on its return from the marine environment to the terrestrial environment of the adult crabs. On the other hand, however, it may only indicate a greater selection by these salinities during zoeal development and have no bearing on greater adaptation of the megalops stage. The role of temperature in controlling the distribution of the species through its effect on the larval stages is apparent from the present study. Gifford (63) indicates that C. guanhumi has been observed as far north as ero Beach, on the East Coast of Florida. Water temperatures along the beaches of the Georgia coast, as well as farther north, fall below C during several months of the year following the peak of spawning of C. guanhumi in October and November. The results of the present study indicate that although development of a small percentage of the zoeal stages can proceed at this temperature the megalops cannot continue development and complete metamorphosis at C. There is no evidence from the present study that the processes which are associated with adaptation of the adult crabs to the terrestrial environment are initiated during larval development. These morphological and physiological modifications must, therefore, take place during the juvenile and transitional phases of the postlarval development. Although a number of aspects of molting in adult Brachyura have been studied, there is little information on the way in which environmental factors other than temperature affect size increments and frequency of molting. Broekhuysen (55) noted that the crab, Hymenosoma, in brackish water showed greater growth during the juvenile stages, as well as larger absolute size than did those crabs found in normal sea-water. n his earlier studies on Carcinides maenas, however, he did not find any salinity-size relationships (Broekhuysen, 36). Working with the land-crab, Gecarcinus lateralis. Bliss and Boyer (64) found that the initiation of molting is delayed when the crabs are exposed to dry sand. Both Gifford (63) and Herreid (67) consider shape of carapace and increase in size for juveniles and adults of C. guanhumi. Data are not available, however, for size increments of the recently metamorphosed crabs or the way salinity may affect size increments at the time of molting. n the present study, size increments of crabs maintained in salinities of 5-35 on 26 November

11 ENRONMENTAL EFFECTS ON CRAB LARAE 409 p.p.t. during the first seven post-larval molts did not show any effects of salinity. n those crabs maintained in fresh water, however, size increments during these same molts were consistently reduced. Most observations on frequency of molting in the Brachyura are estimates based on size groups of large numbers of individual crabs rather than on actual measurements of the same crab before and after ecdysis. There are numerous accounts of the difficulties associated with inducing molting under laboratory conditions. n those few cases where normal ecdysis has been observed in intact crabs, the number of individuals has been extremely small and only one molt was involved. Although the conditions under which the crabs in the present study were maintained differed greatly from those of the natural environment, the observations on frequency of molting were made on the same crabs maintained at one temperature over seven consecutive molts. There was considerable variation in the time of molts one through seven (Table 3), both within the experimental series and between the series. There is no indication, however, that molting frequency was affected consistently by either high or low salinities (Fig. 4). n the series of crabs maintained in fresh water, however, the intermolt period was reduced for each of the first seven molts. Although not necessarily related to the increased frequency of molting, survival of the post-larval stages was also lower in the crabs maintained in fresh water than in any of the other experimental salinities. Tolerance to varying salinities, also found in a number of estuarine crabs, would increase the number of environments that juvenile and adult crabs could utilize in feeding, escaping predators, and generally widening the range of distribution inland from the marine and estuarine environments of the larvae. Juvenile C. guanhumi live, molt, and grow in a wide range of salinities, even fresh water. That this ability has any truly adaptative value in the terrestrial environment, however, can only be assumed. The present study would seem to emphasize one point only: crabs that are successful in occupying a niche in the terrestrial environment as adults still remain totally dependent upon the marine and estuarine environments for spawning, development, and distribution of the larval stages. Although the adults may have been successful in their invasion of land, as evidenced by their very presence there, the larvae upon which the species depends for maintenance and continued expansion of its range continue to remain subject to the numerous ecological variables of the marine environment. REFERENCES Bliss, D. E. 63. The pericardial sacs of terrestrial Brachyura, p n H. B. Whittington and W. D.. Rolfe, (ed.], Phylogeny and evolution of Crustacea. Mus. Comp. Zool., Harvard Univ., Cambridge, Mass. Bliss, D. E., and J. R. Boyer. 64. Environmental regulation of growth in the decapod crustacean Gecarcirws lateralis. Gen. Comp. Endocrinol. 4:-41. Bliss, D. E., S. M. E. Wang, and E. A. Martinez. 66. Water balance in the land crab, Gecarcinus lateralis, during the intermolt cycle. Am. Zoologist 6: Broekhuysen, G. J. 36. On development, growth and distribution of Carcinides tnaenas (Linn ). Arch. Neerl. Zool. 2: Broekhuysen, G. J. 55. The breeding and growth of Hymenosoma orbiculare Desm. (Crustacea, Brachyura). Ann. S. African Museum 41: Cabrera, J. 65. Contribuciones carcinologicas. El primer estadio zoea en Gecarcinus lateralis (Friminville) (Brachyura Gecarcinidae) procedente de eracruz, Mexico. Anales nst. Biol. Univ. Mexico 36:3-7. Cannon, H. G. 23. A note on the zoea of a land-crab, Cardisoma armatum. Proc Zool. Soc. London 23: Costlow, J. D., Jr. 67. The effect of salinity and temperature on survival and metamorphosis of megalops of the blue crab, Callinectes sapidus. Helgolander Wiss. Meeresunters : Costlow, J. D., Jr., and C. G. Bookhout. 60. A method for developing Brachyura eggs in vitro. Limnol. Oceanogr. 5: Costlow, J. D., Jr., and C. G. Bookhout. 62. The larval development of Hepatus epheliticus (L.) under laboratory conditions. J. Elisha Mitchell Sci. Soc. 78: on 26 November

12 410 JOHN D. COSTLOW, JR., AND CAZLYN G. BOOKHOUT Costlow, J. D., Jr., and C. G. Bookhout. 66. The larval development of Ovalipes oceltatus (Herbst) under laboratory conditions. J. Elisha Mitchell Sci. Soc. 82: Costlow, J. D., Jr., and C. G. Bookhout. 68. The complete larval development of Cardisoma guanhumi Latreille in the laboratory. Crustaceana (n press). Costlow, J. D., Jr., C. G. Bookhout, and R. Monroe. 60. The effect of salinity and temperature on larval development of Sesarma cinereum (Bosc) reared in the laboratory. Biol. Bull. 1:3-2. Costlow, J. D., Jr., C. G. Bookhout, and R. Monroe. 62. Salinity-temperature effects on the larval development of the crab, Panopeus herbstii Milne-Edwards, reared in the laboratory. Physiol. Zool. 35: Costlow, J. D., Jr., C. G. Bookhout, and R. J. Monroe. 66. Studies on the larval development of the crab, Rhithropanopeus harrisii Gould.. The effect of salinity and temperature on larval development. Physiol. Zool Costlow, J. 1)., Jr., and E. Fagetti. 67. The larval development of the crab, Cyclograpsus cinereus Dana, under laboratory conditions. Pacific Science 21: de Oliviera, L. 46. Ecological studies on the edible crabs Uca and Guaiamu, Cardisoma guanhumi and Ucides cordatus. Mem. nst. Oswaldo Cruz (Brazil) 44: Gifford, C. A. 63. Some observations on the general biology of the land crab, Cardisoma guanhumi (Latreille) in South Florida. Biol. Bull. 123: Gifford, C. A., and R. F. Johnson. 62. Distribution of calcium in the land crab Cardisoma guanhumi during shell wound recalcification. Comp. Biochem. Physiol. 7: Gross, W. J. 55. Aspects of osmotic regulation in crabs showing the terrestrial habit. Am. Naturalist 89: Gross, \. J. 63. Cation and water balance in crabs showing the terrestrial habit. Physiol. Zool. 36: Gross, W. J. 64. Trends in water and salt regulation among aquatic and amphibious crabs. Biol. Bull. 127: Herreid, C. F. 67. Skeletal measurements and growth of the land crab, Cardisoma guanhumi Latreille. Crustaceana 13: Moreira, C. 13. Embryologie de Cardisoma guanhumi, Latr. Mem. Soc. Zool. France 25: on 26 November

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