The Ecology of Burrowing Decapods (Crustacea)

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Oseana, Volume XXVI, Nomor 4,2001:25-32 ISSN 0216-1877

THE ECOLOGY OF BURROWING DECAPODS (CRUSTACEA)

Oleh

Rianta Pratiwi l)

ABSTRAK

EKOLOGI DARI DEKAPODA YANG HIDUP SECARA MELIANG (KRUSTASEA), Kehidupan secara meliang dari beberapa dekapoda (Krustasea) mempunyai karakteristik tersendiri. Secara fisiologis kehidupan meliang dari setiap jenis krustasea berbeda-beda. Spesies yang hidup di air secara terus menerus berbeda dengan spesies yang hidupnya semi daratan. Strategi meliang dari krustasea dekapoda di beberapa habitat (di perairan air tawar, semi- daratan. dan perairan laut), adaptasi pernafasan di dalam liang habitat serta bagaimana caranya spesies-spesies tersebut dapat mengatasi problem ventilasinya di "branchial chambers" akan dibahas dan diulas secara jelas pada tulisan ini.

INTRODUCTION Semi-terrestrial species are not prima- rily adapted to the challenges a fossorial The burrow-dwelling mode of life is mode of life, but to the challengers of living characteristic of many decapods. In physio- in air. For them, the burrow provides essential logical terms, burrow occupancy presents very protection from adverse physical factors, e.g, different problems to aquatic and semi- temperature and humidity extremes and is terrestrial decapods. Aquatic species, while usually a source of water (ATKINSON & gaining protection from predators when within TAYLOR 1988). their burrows, face potential problems of LITTLE (1983), pointed out that the hypoxia (low oxygen concentration) and relatively large size of burrowing semi- hypercapnia (high carbon dioxide concentra- terrestrial crabs necessitated this mode life tion) and demonstrate appropriate adapta- since there was insufficient protective cover tions. elsewhere in their habitat.

l) Marine Biology Division, Research Centre for Oceanography Indonesian Institute for Sciences, Jakarta.

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Several terms and concepts are dis- The terms "semi-terrestrial and terres- cussed, and burrow function formation and trial" are both used in the decapod literature structure are considered in order to provide a but there is much variation in their applica- basis for subsequent physiological comments. tion and they are often used interchangeably. WARMER (1977) divides decapods into aquatic and semi-terrestrial categories. The TERMS AND CONCEPTS terms terrestrial raises problems since, strictly speaking, no decapod is completely indepen- The most problematic terms are the dent of standing water for breeding, develop- words "burrow and burrowing". FREY (1973) ment and dispersal to adopt the definition defined a "burrow" as an excavation made of POWERS & BLISS (1983). BLISS (1968) within unconsolidated sediment, but excluding used the terms semi-terrestrial and terrestrial intrastratal trails. Whereas the term "burrowing" to categorize decapods that had invaded embraces any animal moving through the land and, although recognizing the difficul- sediment, some produce burrows and other ties posed by those terms. REBACH & do not, the passage of the animal through the DUNHAM (1983) followed this division sediment in the latter case being detected by editorially for marine crabs. Semi-terrestrial the presence of an intrastratal trail. FREY species were considered to be throse, which (1973) started that "trails and burrows" reflect had, ready access to sea-water. fundamentally different behavior and they POWERS & BLISS (1983) now appear generally have diagnostic morphologies. A to reject the term semi-terrestrial in favor of "burrows systems" then refers to a highly grades of terrestrial adaptation since semi- ramified and/or interconnected burrow: a terrestrial covers such a wide adaptation "shaft" is a dominantly vertical burrow or range. They designated five grades of terres- burrow component and a "tunnel" is a domi- trial adaptation based on requirements for nantly burrow or burrow component. standing water and resistance to desiccation. NYE (1974) distinguished between bur- The zones corresponding to the grades were row excavation and rapid burying and pointed mid-littoral, high littoral, supralittoral, out that the two behavior patterns were very extralittoral and terrestrial. This scheme is different, involving different adaptations and marine oriented and, although that authors selection pressures. The words "bury and state that an analogous situation exists for burying" are used below in connection with emergence to land from freshwater habitats, burrowing in connection with burrowing for their scheme does not take proper account of concealment but without burrow formation. this. Burrow contraction is a characteristic HORWITZ & RICHARDSON (1986) of some nantantian decapods e.g. Alpheidae, presented an ecological classification for although it appears that burying behavior is freshwater crayfish based on the proximity of normal for concealment in other shrimp their burrows to water. They considered that families associated with sediments. Among their habitat-orientated scheme reflected the the reptantian decapods, burrow construc- physiological conditions faced by the crayfish. tion is widespread in infraorders Astacidea. Three categories of burrow were recognized: Thalassinidea and Brachyura and burying those in or connected to open water, those behavior is characteristic of many species of connected to the water table and those inde- Brachyura and some species of Anomura pendent of the water table. (ABELE & FELGENHAUER 1982).

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BURROWING, BURROWS AND BUR- Function of burrows ROW FUNCTION A number of functions have been Excavatory behavior and burrow Structure attributed to the burrows of decapod crusta- The burrows and digging behavior of ceans. These include concealment from preda- crabs have been reported by VANNINI (1980) tors, protection from adverse environmental and the burrows of Thalassianids by conditions with the associated provision of DWORSC HAK (1983); for both groups, new micro-environmental stability, provision of information is accumulating rapidly sire for moulting, mating, egg incubation or Nephropid lobsters, crayfish, thalas- juvenile recruitment, provision of a sire for sinids and alpheids excavate their burrows in feeding (either by extraction of food from a broadly similar manner, variously using their within the burrow, or by transport of food to first three pairs of pereiopods and third the burrow, or by feeding adjacent to the maxillipeds to excavate and transport loads of burrow, or by utilizing burrow water in the sediment (MacGINITIE & MacGINITIE 1968; feeding process), access to standing water or GROW 1981; YANAGISAWA 1984). damp conditions in semi-terrestrial species or Decapod burrows range in complexity the provision of oxygenated water "within" from simple shafts or tunnels with a single the sediment in aquatic species and stridula- opening to the surface, e.g. many Uca and tion enhancement in some semi-terrestrial spe- Ocypode species (VANNINI 1980), to complex cies (MACNAE 1968; VANNINI 1980, burrow systems with many surface openings HAZLETT 1983). and extensive branching tunnels e.g some The most fundamental of these func- Nephrops norvegicus burrows with nonspecific associations (CHAPMAN 1980; ATKINSON tions is protection from predators but in semi- 1986) and burrow systems occupied by adult terrestrial species protection from adverse en- and juvenile crayfish of the genus Engaeus vironmental conditions is of great importance. (HORWITZ it. al 1985) (Figure 1).

Figure 1. Decapod burrows, a) Fallicambarus fodiens; b) Engaeus tuberculatus; c) Ocypode cordimana; d) Uca lactea lactea; e) Axius serratus; f) Callianassa subterranean; g) Upogebia pusilla; h) Calocaris macandreae; i) Goneplax rhomboides; j) Alpheus crassimanus; k) Nephrops norvegicus (FINCHAM & RAINBOW 1988).

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THE BURROW ENVIRONMENT: but did point out that remoistening body BEHAVIORAL AND PHYSIOLOGICAL surfaces within the burrow would result in a CONSIDERATIONS period of evaporative cooling when crabs returned to high temperatures at the surface. Semi-terrestrial species Here, colour changes and orientation could The physiological adaptations of semi- also be effective in thermoregulation. It is terrestrial borrowers are essentially adapta- clear, however that the burrow provide pro- tions to life on land rather than to life in a tection from lethal extremes of temperature. burrow and are principally concerned with POWERS & COLE (1976) also studied salt and water balance (POWERS & BLISS temperature variation in microhabitats, includ- 1983; LITTLE 1983). ing burrows, occupied by species of Uca and EDNEY (1961, 1962) investigated the concluded that burrows provided a major water and heat relationships of five tropical heat refuge for Uca panacea on Texan barrier species of Uca, which occupied progressively island sand flats. Air inside a typical burrow more terrestrial habitats. Each species had a showed an initial rapid drop in temperature sharply defined upper lethal temperature (43.3 with increasing depth followed by a more ° C for the most terrestrial species) which out gradual decrease with the lowest temperature of burrow ground temperatures could exceed. at the deepest portion of the burrow. In one Evaporative water losses depressed body tem- examples, air temperature in the burrow lumen peratures but crabs could retreat into their was around 25°C at 25 Cm depth compared burrows if conditions became extreme. There, with 35°C at the burrow entrance. Burrow temperatures were much cooler and burrows temperature at night was some 5°C warmer reached the water table so that there was no than surface temperatures open the margin danger of desiccation. In one example the between life and death POWERS & COLE burrow temperature at about 30 cm depth was (1976). During cold periods crabs remained 26 °C compared with an outside air tempera- within plugged burrows. It was also observed ture of 30.0 - 32.5°C and a soil surface tem- that the daily heat wave reached the bottom perature of 44.5 - 46.4°C. When within the of burrows about 5 hours later and could burrow, crab body temperature equaled in elevate the temperature sufficiently to pro- burrow air temperature, but measurements voke nocturnal winter activity. close to upper lethal limits were recorded At Kuala Selangor on the Malaysian from crabs on the sediment surface. peninsula, MACINTOSH (1978) reported that SMITH & MILDER (1973) suggested the mean monthly air temperatures varied by that solar heating could increase burrow tem- less than 2°C and that the mean diel variation peratures on clear winter days when air tem- was 9°C. Although differences in soil surface perature was low. During cool, overcast spring temperatures were recorded, the temperatures and winter days the crabs remained within within burrows of Uca spp. were similar on their burrows. In January, crabs that were different parts of the shore and temperature unable to burrow deeply, because of underly- was constant at 28 - 30°C at a depth of 10 Cm. ing rock, died. Since body temperature Where the soil surface temperature showed a changed very rapidly, SMITH & MILLER diel fluctuation of 14°C, burrow temperature (1973) did not consider the feeding burrow fluctuation by only 3°C. Although mud sur- retreat rhythm described by WILKENS & face temperatures could exceed the thermal FINGERMAN (1965) to be thermoregulatory tolerance of the crabs, MACINTOSH (1978)

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concluded that the primary function of the conditions and possess respiratory adapta- burrow of mangrove Uca spp. was no replace tions which enable them to maintain oxygen water losses and that thermoregulatory uptake under these conditions, obviating the advantage was coincidental. The stimulus for need to irrigate the burrow continuously. replacing water was considered to be feeding Many species of decapod Crustacea rather than the replacement of evaporative are able to keep their rate of oxygen uptake losses. constant over a wide range of PO-,. This Equivalent information on semi-terres- ability is particularly well developed among trial burrowing crayfish is scarce and little is burrowing species. Although these animals known about their burrow environment or are well adapted for anaerobic metabolism, about their burrow-oriented behaviour and FELLER (1979) has suggested that they may physiological adaptation. also use aerial respiration to enable them to survive the extreme conditions within the Aquatic species burrows during low tide. This is supported The burrowing habit adopted by many by the observations of FARLEY & CASE semi-terrestrial crabs affords them a consider- (1968) who reported that Callianasa able degree of protection against extremes of californiensis may move towards the environmental conditions. This is probably openings of its burrow at low tide. More also true for some species of crayfish during recently, HILL ( 1981), in a study of three periods when their burrows do not contain species of Upogebia from South Africa, has standing water, since relative humidity is likely shown that all three species may move up to to remain high. For aquatic decapods, how- the air/water interface in the burrow at low ever the situation is rather different. While tide. None of the species left the water these species will gain by reducing the risk of completely but each took up a position in predation, they are faced with the problem of which water could be pumped through the gill coping with the reduced partial pressure of chamber even though the cephalothorax was oxygen (PO2) of the water within the burrow. above the water level. Hypoxic conditions within the burrow result from the oxygen consumption not only of the occupant but also of the microflora and PHYSIOLOGICAL PROBLEMS meiofauna lining the burrow. Since the PO2 of the ASSOCIATED WITH BURYING water overlying the sediment is normally much higher than that of the burrow water, oxygen Decapods which bury themselves in could diffuse into the burrow but. because the soft sediments face a number of problems, diffusion rate of oxygen in water is very much perhaps the most important of which is the slower than in air, this process alone could not maintenance of a flow of water through the maintain the PO2 of the water in the burrow at branchial chambers for respiratory purposes. normoxic level. The magnitude of this problem will depend, Since the energy cost of pleopod ven- of course, on the extent to which the animal tilation is likely to be high, intermittent irriga- is buried in the substratum. tion of the burrow may represent a behavioural In many shallow-burying species of adaptation to reduce these coasts to mini- crab, the chelipeds are held close to the body mum levels. The majority of burrowing spe- and create channels between the chelipeds cies studied are highly tolerant of hypoxic and the body, which enable a current of water to be drawn down towards the main openings

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emerging mainly at night. Diurnal emergence is usually associated with frequent return visits to the burrow for the replenishment of body water. The burrow environment enables crabs to avoid environmental stresses by of branchial chambers at the bases of the behavioural means. In addition, semi-terres- chelipeds in the normal manner. This trial decapod shows physiological adapta- behaviour has been noted in a number of tions to cope with both the problems of aerial crabs, e.g. Carcinus maenas and Liocarcinus respiration and salt and water balance, depurator. but such adaptations are not exclusive to Some crabs, such as Corytes burrowers. cassivelaunus and Atelecyclus rotundatus, Although aquatic decapods which however may bury themselves much deeper have adopted the burrowing habit also gin by in the substratum so that they are unable to reducing the risk of predation, these species use the above behaviour to maintain a supply must be adapted to cope with the reduced of water to the branchial chambers. oxygen content (and increased carbon diox- Burying behaviour also occurs in many ide content) of the water within their burrows. shrimps. For example, in Crangon crangon Freshwater crayfish appear to fall somewhere the animal frequently buries itself in sand just between these two categories and further deep enough to cover the antennal scales information on their physiological ecology is leaving the eyes protruding above the sur- required in order to extend out understanding face of the substratum. The animal creates a of the range of adaptations to a burrowing small inhalant and exhalant opening on either mode of life among the decapod Crustacea. side of the body at the bases of the antennal scales. Either opening can operate as the inhalant or exhalant opening and water is REFERENCES drawn down to the ventral surface of the body by the action of the scaphognathite ABELE, L. G. and B. E. FELGENHAUER 1982. and is directed into the branchial chambers at Decapoda. In Synopsis and classi- the ventral edge of the brachiostegite. Exhal- fication of living organisms. PARKER, ant water is then directed away from the body S.P. (Ed). Me. Graw-Hill Book, Co, New via the exhalant opening. York. 2: 296-326. Animal which bury into soft sediments are unlikely to experience the degree of ATKINSON, R.J.A. 1986. Mud burrowing hypoxia that burrow-inhabiting species do megafauna of the Clyde Sea Area. Proc since they attempt to maintain access to the R. Soc. Edinb. 90 B. 351-361 . water above the sediment surface, which normally has a high oxygen content. ATKINSON, R.J.A. and A. C. TAYLOR 1988. Physiological ecology of burrowing decapods. Symp. zool. Soc. CONCLUSIONS Lond, 59: 201-226.

Many decapods have adopted a bur- BLISS, D. E. 1968. Transition from water to rowing mode of life and derive various ad- land in decapod crustaceans. Am. Zool. vantages as a result. 8 : 355-39 2. The burrows of semi-terrestrial crabs provide a refuge from extreme environmental conditions. There are many patterns of burrow emergence, but a frequent feature is to avoid the warmest hours of the day by

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CHAPMAN, C. J. 1980. Ecology of juvenile FREY, R.W 1973. Concepts in the study of and adult Nephrops. In The Biology biogenic sedimentary structures. J. and management of lobsters, 2 sedim. Petrol, 43: 6-19. Ecology and management. COBB, J.S. & PHILLIPS, B.F. (Eds.), Academic GROW, L 1981. Burrowing behavior in the Press, New York London: 143-148. crayfish, Cambarus diogenes Girard. Anim. Behav. 29:351-356. DWORSCHAK, P.C. 1983. The biology of Upogebia pusilla (Petagna) (Decapoda, HAZLETT, B. A. 1983. Parental behavior in Thalassinidea). 1. The burrows, Pubbl. decapod Crustacea. In Studies in Staz. zool. Napoli (Mar. Ecol.) 4 :19- adaptation: The behavior of higher 43. Crustacea. REBACH, S & DUNHAM (Eds). John Wiley & Sons, New York. EDNEY, E.B. 1961. The water and heat rela- 171-193. tionships of fiddler crabs (Uca spp.) Trans. R. Soc. S. Afr; 36: 71-91. HILL, B. 1981. Respiratory adaptations of three species of Upogebia (Thalassi- EDNEY, E.B. 1962. Some aspects of the tem- nidea, Crustacea) with special re- perature relationships of fiddler crabs ference to low tide periods. Biol. Bull. (Uca spp.). In Biometeorology: Marr. biol. Lab. Woods Hole, 160: TROMP, S.W (Ed), Pergamon Press, 272-279. Oxford. 79-85. HORWITZ, P.H.J., RICHARDSO, A.M.M. and FARLEY, RD. and CASE, J.F.1968. Perception of BOULTON, A. 1985. The burrow habitat external oxygen by the burrowing of two sympatric species of land shrimp Callianassa californiensis crayfish, Engaeus urostrictus and E. Dana and C.affinis Dana. Biol Bull. tuberculalus (Decapoda. Parastacidae). Mar. biol. Lab. Woods Hole, 134: 261- Viet. Nat. 102: 188-197. 265. LITTLE, C. 1983. The colonization of land. FINCHAM, A.A. and P.S. RAINBOW 1988. Origins and adaptations of terrestrial Aspect of Decapod Crustacean Biology. animals. Cambridge University Press, The Proceedings of a Symposium held Cambridge. 211 pp. at the Zoological Society of London on 8th and 9th April 1987. The Zoological MacGINITE, G. E. and MacGINUTIE, N. 1968. Society of London, Clarendon Press, Natural history of marine animals, Oxford, 376 pp. (2nd edn). McGraw-Hill Book Co., New York. FELDER, D.L. 1979. Respiratory adaptations of the estuarine mud shrimp, MACNAE, W. 1968. A general account of the Callianassa jamaicense (Schmitt, 1935) fauna and flora of mangrove swamps and (Crustacea, Decapoda, Thalassinidea). forest in the Indo-West-Pacific region. Biol. Bull. mar. biol. Woods Hole, Adv. Mar. Biol. 6: 73-270. 157: 125-137.

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VANNINI, M.1980. Researches on the coast POWERS, L. W., and D. E. BLISS. 1983. Ter- of Somalia. The shore and the dune of restrial adaptations. In The Biology Sar Uanle. 27. Burrows and digging of Crustacea. 8. Environmental adapta- behavior in Ocypode and other crabs tions. VERNBERG, F. J and VERNBERG (Crustacea, Brachyura). Monitore zool. W.B (Eds), Academic Press, New York. Ital (N. S) (Supply. 13: 11-44. 271-333. WARNER, G. F. 1977. The biology of crabs. POWERS, L.W., and COLE, J.F. 1576. Tem- Elek Science, London. 196 pp. perature variation in fiddler crab microhabitats. J. Exp. Mar. Biol. WILKENS, J.L., and FINGERMAN, M. 1965 Ecol. 21: 141-157. Heat tolerance and temperature relationships of the fiddler crab, Uca REBACH, S. and D. W. DUNHAM. 1983 pugilator, with reference to body Studies in adaptation : The behavior coloration. Biol. Bull. mar. biol. Lab. of higher Crustasea. John Wiley & Woods Hole. 128: 133-141. Sons, New York. 223 pp. YANAGISAWA, Y. 1984 Studies on the inter- SMITH, W. K. and MILLER P.C. 1973. The specific relationship between gobliid thermal ecology of two South Florida fish and snapping shrimp. II. Life fiddler crabs: Uca rapax Smith and history and pair formation of snap- Uca pugilator Bosc. Physiol, Zool, ping, shrimps Alpheus bellulus. Publs. 46: 186-207. Seto. Mar. biol. Lab. 29: 93-116.

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