OCEANOLOGICA ACTA- VOL. 19- W 3-4 ~ -----~-

Dis turban ce The effect of sublethal predation Predation Sublethal predation on the biology of echinoderms Echinoderms Perturbation Prédation Prédation sublétale Echinoderme

John M. LA WREN CE a and Julio VASQUEZ b

a Department of Biology, University of South Florida, Tampa, FL 33620, U.S.A.

b Departamento de Biologia Marina, Universidad Cat6lica del Norte, Coquimbo, Chile.

Received 17/01/95, in revised form 08/01196, accepted 11101196.

ABSTRACT In contrast to plants, predation on animais is usually lethal. Analysis of the effect of predation on animal populations and on predator-prey dynamics typically assumes this is the case. However, sublethal predation occurs in echinoderms, primarily on the arms of crinoids, asteroids, and ophiuroids. Sublethal predation is important in the se echinoderms as it meets one of Harris' ( 1989) major crite­ ria, affecting basic biological processes such as acquisition of food and allocation of nutrients to growth and reproduction. Sublethal predation would have an effect on their ecological role. It is essential to consider sublethal predation in the analysis of the life-histories of these species.

RÉSUMÉ Les effets de la prédation sublétale sur la biologie des échino­ dermes.

A l'inverse de la plante, l'animal subit une prédation qui lui est habituellement mortelle. Ceci est confirmé par la plupart des analyses de prédation au sein des populations animales et de la dynamique prédateur/proie. Cependant une préda­ tion sublétale c'est-à-dire sans effet fatal, existe chez les échinodermes, principa­ lement chez les crinoïdes, astéries et ophiures. Pour répondre à cette définition, ce genre de prédation doit répondre au critère de Harris ( 1989) c'est-à-dire influencer les processus de base tels que la croissance et la reproduction et varier en fonction de la densité de la population en cause. L'existence de cette préda­ tion et ses conséquences chez les échinodermes ont été rarement étudiées. Pour certaines espèces, cette prédation peut avoir un impact important sur leur biolo­ gie et donc sur leur rôle écologique. Il est essentiel de prendre en compte ce genre de prédation lors d'une analyse des cycles de vie des échinodermes.

Oceanologica Acta, 1996, 19, 3-4,431-440.

INTRODUCTION This contrasts to herbivory, which is usually sublethal (Harper, 1977). Predation can be lethal or sublethal. Sublethal predation is Is sublethal predation important ? The costs of sublethal the consumption by a predator of a portion of the prey's predation are direct in the loss of biomass and indirect in biomass that does not result in death. The Joss of biomass the Joss of function. Thus both the amount of a structure is defined as disturbance (Grime, 1977; Sousa, 1984; Wit­ Iost and the importance of the structure in the function of man, 1985; Tilman, 1988; Pickett et al., 1989). In the case the organism are important (Harper, 1977). Regeneration of carnivory, predation is usually lethal (Taylor, 1984). of the lost parts may follow sublethal predation and would

431 J. M. LAWRENCE, J. VASQUEZ be an additional cost. Regeneration implies the structure tai pinnules. The potentialloss of gamete production could involved is important but not essential according to Goss' be calculated from these data. Similar calculations could be (1969) paradigm, and that the benefits of regeneration made for the loss of gametes with arm loss in asteroids. exceed the cost. Reichman's (1984) support of Goss's This bas not been done. paradigm did not consider the consequences of allocation Lane (1984) suggested the large anal sac of extinct inadu­ of resources to regeneration on other functions of the orga­ nates contained the gonads, separating them from the nism, which provides the potential for a classical trade-off remaining viscera. Disadvantageous as the Joss of the between the use of limited resources for competing uses. gonad intuititively seems, Lane hypothesized it was adap­ Although the effect of herbivory on the biology of plants tive in these crinoids by suggesting the supposed extra-the­ and the dynamics of animal-plant interactions bas long cal location of the gonad was an evolutionary adaptation to been studied (Crawley, 1983), the effect of sublethal pre­ attract sublethal predation to the gonads to spare the vital dation on the biology of animais bas not. lt affects growth organs in the theca. in crustaceans (Bennett, 1973; Kuris and Mager, 1975; In extant crinoids, the gonads are located in the arms or in Smith, 1990), bivalves (Peterson and Quammen, 1982; genital pinnules (Hyman, 1955). Noting the high incidence Trevallion, 1971; Trevallion et al., 1970; Kamermans and of sublethal predation on the arms and pinnules of Antedon Hui tema, 1994 ), and polychaetes (de V las, 1979), and bifida, Nichols (1994) like Lane suggested the occurrence reproduction in polychaetes (Zajac, 1985). of the gonads on the arms was a strategy of tolerating Harris ( 1989) proposed sublethal predation is an important sublethal predation of the pinnules to protect the more vital factor regulating population size, providing the criteria of organs in the theca. Nichols stated such a strategy would density-dependency and depression of long-term survival be justified only if the loss and regeneration could be equa­ and reproduction are met. If so, it would be expected to ted in energy terms, and that lifetime reproductive potential have evolutionary consequences as Vermeij (1982, 1987; must be considered. Aronson, 1994) suggested. Sublethal predation in echinoderms bas been documented Effect on nutrient reserves in relative] y few studies; it bas been presumed in a number Essentially ali tissues of echinoderms are used if starvation of studies (Tab. 1 ). lt is most common in the stellate is sufficiently extensive. The pyloric caeca of asteroids are classes whose arms are both susceptible to predation and specifie reserve organs (Giese, 1966; Lawrence and Lane, capable of wound healing. Although these data indicate 1982; Lawrence, 1987). Sublethal predation on the arms of sublethal predation occurs, they should not be taken as evi­ asteroids wou1d decrease the amount of reserves. This dence that it occurs in all taxa in these groups. Arm loss would decrease the ability of the individual to withstand and regeneration have never been found in sorne asteroid starvation and the amount of reserves that cou1d be used for species (Lawrence, 1992). Sorne have extremely protective gametogenesis. As with the gonads, the amount of nutrient body-walls (Blake, 1991) and others have large coelomic reserve lost with arm loss can be calculated. This bas not cavities that cannot be sealed. The incidence of arm loss been done. can be extremely variable in those species in which it does occur (Lawrence, 1992). The large coelomic cavity and rigid tests eliminate the possibility of sublethal predation in Effect on movement regular echinoids or spatangoids (Emson and Wilkie, When attacked by the asteroid Solaster dawsoni, the aste­ 1980) as any substantial rupture of the test should result in roid Pycnopodia helianthoides autotomizes arms and death. However, sublethal predation of the edges of the escapes (Birkeland et al., 1982). Not on1y is the behavior tests of clypeasteroids occurs. Sublethal predation on the of the individual affected, but that of others as weil as they tube feet and pedicellariae have been reported. show an alarm response to the presence of body and tissue The costs of sublethal predation in echinoderms and, as fluids of their conspecifics. The asteroid Stichaster striatus Emson and Wilkie ( 1980) observed, "the effect of the bur­ also autotomizes arms when attacked, but does not show den of regeneration on growth, reproductive potential, and an a1arm response (Lawrence, unpub. obs.). This may be general viability, are not weil known". Here the biological rsponsible for a much higher rate of sublethal predation effects of sublethal predation on echinoderms will be (Viviani, 1978). considered. These effects must be known to fully unders­ Hiding time did not change with arm loss in Microphio­ tand the ecology and evolution of the species in which it pholis gracillima, as individuals usually travelled down an occurs, and in the analysis of their life histories. existing hole rather than burrowing (Clements, 1985). Gro­ ber (1988 a) reported that the time for withdrawal into the reef by the ophiuroid (Ophiopsila riisei) is significantly Effects of sublethal predation increased immediately following arm loss. The ophiuroid Effect on reproduction Ophioderma brevispina with two or three lost arms do not move as rapidly as intact individuals until arms regenerate A direct effect on reproduction occurs if sublethal preda­ to halfthe length ofthe intact arms (Henry, 1993). tion results in loss of gonads. This would occur with arm Joss in crinoids and asteroids and with visceral-mass loss in Effect on acquisition of nutrients ophiuroids. Nichols ( 1994) reported the average loss of pinnules of the crinoid Antedon bifida was 17 % and that Sublethal predation may decrease production by decrea­ sublethal predation was almost totally confined to the geni- sing the acquisition of nutrients (feeding and digestion). As

432 SUBLETHAL PREDATION IN ECHINODERMS

Table 1 71 % of individuals and 8 %of ali arms regenerating (Schneider, Studies documenting or presuming sublethal predation in echino­ 1988). Arms preyed upon by the fish Chaetodon ephippium (Meyer derms. et al., 1984). Himerometra bartschi: 2 % with regenerating visceral mass; 67 % Class Crinoidea with regenerating arms (Meyer, 1985). Order Isocrinida Lamprometra pa/mata: 40 % of individuals and Il % of ali arms Cenocrinus asterias: Lost arms almost always few in number and regenerating (Schneider, 1988). partially regenerated (Messing et al., 1988). Nemaster grandis: JOO% of individuals and 13% of ali arms regene­ Diplocrinus wyvillethomsoni: Photographs show fish feeding on arms rating (Schneider, 1988). (Conan etal., 1981). Oligometra serripinna: ca. 30 % of population with arm Joss (V ail, Metacrinus fossilis: !0 % arm regeneration in specimens of this 1989). extinct species is lower than that of modem isocrinids living deeper Pontiometra andersoni: 100 % of individuals and 15 % of ali arms than 100 rn (Meyer, Oji, 1993). regenerating (Schneider, 1988). Metacrinus rotundus: 89 % of individuals with arm regeneration Reometra mariae: 100% of individuals and 14% of ail arms regene­ (Meyer, Oji, 1993). rating (Schneider, 1988). Stephanometra indica: 24 % of individuals and 3 % of ali arms rege­ Order Comatulida nerating (Schneider, 1988). "comatulids": The triggerfish Ballistoides conspicillum observed Stephanometra oxyacantha: 4 % with regenerating visceral mass; attacking arms of partially exposed individuals. Feces contains por­ 33 % with regenerating arms (Meyer, 1985). tions of crinoid arms (Gladstone, in Vail, 1987). Tropiometra afra: 21 %of individuals and 5% of ali arms regenera­ Antedon bifida: Predation on pinnules by wrasse Crenilabrus melops ting (Schneider, 1988). (Nichols, 1994).

Capil/aster sp.: 3 % with regenerating visceral mass; 32 % with rege­ Class Asteroidea nerating arms (Meyer, 1985). Capillaster multiradiatus: 4 % with regenerating visceral mass; 29 % Order Forcipulatida with regenerating arms (Meyer, 1985). 44% of individuals and 6 % Asterias amurensis: Arm Joss possibly from predation by the crab of ali arms with regeneration (Schneider, 1988). Paralithoides camtschatica (Hartsock, pers. comm.). Cenometra bella: 6 % with regenerating visceral mass; 50 % with Asterias forbesi: 10 % of the spider crab Libinia emarginata with arm regenerating arms (Meyer, 1985). JO % of individuals and JO % of ali ossicles in stomach (Aldrich, 1976). arms regenerating (Schneider, 1988). Asterias rubens: Arms autotomized in response to predation by the Colobometra perspinosa: 9 % with regenerating visceral mass; 23 % stone crab Hyas araneus and the asteroid Solaster papposus (Han­ with regenerating arms (Meyer, 1985). cock, 1955, 1974). Arms autotomized in response to predation by the Comanthina sp.: 63 % with regenerating arms (Meyer, 1985). ast~roid Solaster endeca (Christensen, unpub., in Feder and Christen­ sen 1966). lndividuals in the eastern Bering Sea often missing arms, Comanthina schlegeli: 5 % with regenerating visceral mass; 65 % presumably from predation (possibly crab Paralithoides camchatica). with regenerating arms (Meyer, 1985). 68 % of individuals and 4 % As often only distal portions of arms missing, probably cropping and of ali arms regenerating (Schneider, 1988). not autotomy (F. Hartsock, pers. comm.) Comanthus parvicirrus: 3 % with regenerating visceral mass; 33 % Asterias vulgaris: Il % with regenerating arms (King, 1898). Arms with regenerating arms (Meyer, 1985). lost to attack by lobsters in the laboratory (Breen, 1974). Comaster bennetti: 1.8 % with regenerating visceral mass Evasterias troscheli: Arms autotomized in response to predation by (Meyer,l985). 89 % of individuals and 6 % of ali arms regenerating the asteroid Solaster dawsoni (Christensen, unpub., in Feder and (Schneider, 1988). Christensen, 1966). Predation by S. dawsoni observed (Birkeland et Comaster distinctus: 57 % of individuals and 10 % of ali arms rege­ al., 1982). nerating (Schneider, 1988). Heliaster helianthoides: 0-62 % regenerating arms in different popu­ Comaster multifidus: 63 % of individuals and 3 % of ail arms regene­ lations. Predation by the asteroid Meyenaster gelatinosus. Usually rating (Schneider, 1988). 3-4 adjacent arms regenerating (Viviani, 1978). Comatula purpurea: 16% of individuals and 3 %of arms regenera­ Meyenaster gelatinosus: Predation by the asteroid Luidia magellani­ ting (Schneider, 1988). ca. 10-62 % regeneration in different populations. Occurred in indivi­ duals radius from 80-220 mm, suggesting lethal predation at small Comatheria briareus: 15 % of individuals and 81% of ali arms rege­ size and escape from predation at large size (Viviani, 1978). nerating (Schneider, 1988). Dichrometra flagellata: 83 % of individuals and 5 % of ali arms rege­ Pycnopodia helianthoides: Autotomizes arms in laboratory in respon­ nerating (Schneider, 1988). se to predation by Solaster dawsoni (Mauzey et al., 1968). Feeding by S. dawsoni on autotomized arms observed in field (Birkeland et Florometra serratissima: 80 % with regenerating arms. Although al., 1982). Autotomy of two adjacent arms in response to attack by sorne arm loss attributed wave action and physical factors, most attri­ S. dawsoni (M. Byrne, unpub. obs.). buted to predation by the asteroid Pycnopodia helianthoides and the crab Oregonia gracillis (Mladenov, 1980, 1983). Stichaster striatus: 2-38 % with regenerating 1-2 arms. Occurred in. individuals with radius from 40-90 mm, suggesting lethal predation at · Heterometra savignyi: Suggests arm Joss is the result of fish feeding small size and escape from predation at large size (Viviani, 1978). on plankton trapped in mucus in food grooves. Arm Joss greater in seagrass meadows than in areas where diurnal crypsis is possible Order Valvatidae (Magnus, 1963). Acanthaster planci: Penned individuals often responded to attack by Himerometra magnipinna: 100% of individuals and 24 % of ali arms chiton Charonia tritonis by autotomizing arms (Chesher, 1969). regenerating (Schneider, 1988). Scars on arms attributed to predation (Campbell and Ormond, 1970). Himerometra robustipinna: 5 % with regenerating visceral mass; Arm loss attributed to predation by the triton (Endean, pers. comm.) 77 % with regenerating arms (Meyer, 1985). and fish (Ormond, 1971 ). Predation by shrimp Hymenocera picta and

433 J. M. LAWRENCE, J. VASQUEZ crustacean defensive interactions (Glynn, 1982 b). Arm Joss most Ophiocoma wendtii: 29 % of arms regenerating (Sides, 1987). common at intermediate size (McCallum et al., 1989). Ophiocomina nigra: The hermit crab Pagurus bernhardus eats of arm tips (Gorzula, 1976, in Warner, 1986). 30-54% arm regeneration Order Paxillosida in different populations (Aronson, 1989). Astropecten articulatus: 0-40% individuals regenerating arms (Hop­ Ophioderma appressum: 44 % of arms regenerating (Sides, 1987). kins et al., 1990). 30-74 % arm regeneration in different populations, 50-85 % dise Luidia clathrata: 12-59 % individuals regenerating arms (Hopkins et regeneration (Aronson, 1991 ). al., 1990). Ophioderma brevispinum: 46-57 %, 68 % arm regeneration in diffe­ Luidia magellanica: Predation by the asteroid Meyenaster gelatino­ rent populations (Aronson, 1987, 1991 ). Regenerating arms attributed sus. 51-69 % regenerating in different populations (Viviani, 1978). to water activity and predation (Henry, 1993). Ophioderma cinereum: 34% of arms regenerating (Sides, 1987). Order Velatida Ophiolepis ailsae: 43 % of population regenerating arms (Hendler Solaster stimpsoni: arm stumps or very short arms believed result of and Turner, 1987). predation by Sola.~ter dawsoni; variation in frequency of individuals with arms regenerating directly correlated with abundance of S. daw­ Ophiolepis gemma: high incidence of regenerating arms attributed to soni (Engstrom, 1974). predation or physical factors (Hendler and Turner, 1987, Hendler et al., 1995). Class Ophiuroidea Ophiolepis impressa: 28 %of arms regenerating (Sides, 1987). "ophiuroids": Freshly cropped arms of "ophiuroids" found in guts of Ophiolepis pawsoni: Arm regeneration attributed to predation (Hend­ tiger prawns Penaeus esculentus and Penaeus semisulcatus (Wassen­ ler, 1988). berg and Hill, 1987). "Ophiuroid" vertebrae a dominant prey of nek­ Ophiomusium lymani: Predation by fish bites indicated large number tobenthic crab Portunus pelagicus (Williams, 1982). with evidence of healed lesions in the interradial area over the gonad (Gage and Tyler, 1982). Order Phrynophiurida Ophionephthys limnicola: 79 %of population regenerating arms (Sin­ Asteroporpa annulata: 20 % regeneration of arms (Hendler et al., gletary, 1970, 1980). 1995). Ophionereis reticulata: 74% of arms regenerating (Sides, 1987). Ophiomyxa flace ida: 48% of arms regenerating (Sides, 1987). Ophiophragmus filograneus: Dises in guts of 24 % of the stingray Order Ophiurida Dasyatis sabina (Turner et al., 1982). Acrocnida brachiata: 70 % of ali arms regenerating in intertidal and Ophiopsila riisei: Low leve! of arm Ioss attributed to bioluminescen­ subtidal predation (Bourgoin and Guillou, 1994 ). ce that deters predation by nocturnal portunid crabs (Grober 1988 a, b, c). Amphipholis squamata: 80 % arm Joss, 3 % dise Joss in population (Martin, 1968). 61 % of population regenerating one or more arms, Ophiothrix fragilis: Portions of arms usually found in guts of the her­ ca. 1 % of population regenerating one arm; autotomy of arms more mit crab Eupagurus bernhardus, the swimming crab Macropipus likely from hydrodynamic conditions than predation (Alva and Jan­ puber, the poor cod Gadus minutas, Callionymuys lyra, and Pleuro­ goux, 1990). nectes platessa. Rare for dise to be found. Asterias rubens also ingests anns (Warner, 1971). 27-92% arm regeneration in different Amphioplus coniortodes: 87 % of population regenerating arms, 3 % populations (Aronson, 1989). regenerating dises (Singletary, 1970, 1980). Ophiophragmus filograneus: 52-94 % regenerating arms (Clements Amphiura chiajei: 93 % of adults with arm regeneration (Buchanan, et al., 1994 ). 1964). Pound in 58% of guts of haddock Melanogrammus aeglefinus, 46 % as arms only (Mattson, 1992). 99 % of adults with Ophiothrix lineata: Arm Joss attributed to predation (Hendler, 1984). arm regeneration, 0.5 % with dise regeneration; ali 5 arms of indivi­ Ophiothrix oerstedi: Arm fragments found in feces of polychaete duals regenerating in 65 % of population; attributed to fish predation Eunice rubra, in stomach of ophiuroid Ophioderma brevispina, and (gobi Lesueurgobius friesii, plaice Pleuronectes platessa, flounder the crab Mithrax (Aronson and Harms, 1985). 30-85% arm regenera­ Platichthysflesus, dab Limanda limanda) (Munday, 1993). tion in different populations (Aronson, 1987, 1992). Amphiura filiformis: 84 % of adults with arm regeneration; Joss of an Ophiura spp.: dise and arm fragments frequent in the guts of Ophiura arm causes a brilliant flash and retraction of other arms (Buchanan, texturata, possibly from ingestion of intact individuals (Feder, 1981 ). 1964). 78% arm regeneration, 3% dise regeneration attributed to pre­ Ophiura albida: Ann fragments in gut of hydroid Hydractinia echi­ dation by the young of flatfish (dab and plaice) (Bowmer and Keegan, nata. Autotomizes arm to hydroid in laboratory (Christensen, 1967). 1983). 96% of adults with arm regeneraton attributed to fish (dab L. limanda) (Duinevelt and Van Noort, 1986). Found in 86% of guts of Ophiura sarsi: 39->98 % arm regeneration; arm Joss not size depen­ haddock Melanogrammus aeglefinus, 53 % as arms only (Mattson, dent (Fuji ta, 1992). Arm fragments in gut of plaice Hippoglossoides 1992). High percentage arm regeneration (Skôld et al., 1994). platessoides; <10 % arm regeneration in population (Packer et al., 1994). Hemipholis gracilis: At !east 25 % of ali arms regenerating, greater for large individuals attributed to predation by portunid crab Calli­ nectes arcuatus (Lee and Lee, 1978). Class Echinoidea Microphiopholis gracillima: 77 % of population regenerating arms, Order Echinoida (Singletary, 1970, 1980). 85% of ali arms regenerating attributed to predation (Stancyk et al., 1994). (Note: Hendler et al., 1995, reject Echinometra lucunter: the goby Ginsburgellus novemlineatus feeds Microphiopholis and assign this species to Amphipholis.) primarily on the tube feet and pedicellariae (Teytaud, 1971, in Shir­ ley, 1982). Ophiacantha fidelis: Guts of the asteroid Meyenaster australiensis with arm fragments only (Biaber et al., 1987). Order Clypeasteroida Ophiocoma pumila: Fish (wrasses Halichoeres bivittatus, H maculi­ Dendraster excentricus: Predation on edge of test by crabs Loxorhyn­ pinna, H. garnotti) ate primarily arms of individuals exposed in the cus grandis and Cancer sp. (Merrill and Hobson, 1970). < 5 % of field (Hendler, 1984). 55 % of arms regenerating; Joss attributed to population with broken, healed edges attributed to crab predation predation (Sides, 1987). (Birkeland and Chia, 1971).

434 SUBLETHAL PREDATION IN ECHINODERMS

Hymenocera picta on the asteroid Acanthaster planci range Me/lita quinquiesperforata: Regenerating edge of test attributed to predation by crab Callinectes sapidus or fish, although possibly from from minor wounds to massive wounds with arms missing wave damage (Weihe and Gray, 1968). (Glynn, 1982, 1984). Subsequently, the scavenging poly­ chaete Pherecardia striata enters the wound and causes death of the asteroid by feeding on the internai organs. C1ass Holothuroidea Glynn concluded the combined effect of the shrimp and Order Aspidochirotida polychaete can be a control of populations of A. planci. Stichopus chloronotus: In the Iaboratory, escaped attack by the gas­ Pycnopodia helianthoides apparently damaged by partial tropod Tonna perdix by shedding a piece of the body wall and boun­ digestion by Solaster dawsoni was observed scavenged by ding away (Kropp, 1982). a "host" of the amphipod Parapleustes pugettensis (Eng­ Stichopus horrens: ln the laboratory, escaped attack by the gastropod strom, 1974). Tonna perdix by shedding a piece of the body wall and bounding Whether sublethal predation leads to infection and subse­ away (Kropp, 1982). quent death has never been evaluated, although Birkeland and Lucas (1990) suggested A. planci may be prone to Order Dendrochirotida infection after damage due to its relatively large regions of Athyonidium chilensis: Regenerating tentacles attributed to fish pre­ soft tissues and body cavities. The relation between dation (Vasquez, unpub. obs.). amount of arm loss and survivorship of stellate echino­ Eupencta fraudatrix: Regenerating tentacles attributed to fish preda­ derms in the field has not been documented. tion (Levin, unpub. obs.).

Effect on production the amount of nutrients acquired determines the amount The resources allocated to regeneration and other activities available for ail requirements by the organism, this compo­ add another dimensio~ to the classical growth-reproduction nent of the energy budget is of paramount importance and trade-off. could be a major consequence of sublethal predation. Regenerating tissue can be a large proportion of the body Although dissolved organic material can contribute to of ophiuroids. lt averaged 25 % in Amphiura filiformis in these requirements (Bamford, 1982; Smith et al., 1981; Galway Bay (Bowmer and Keegan, 1983) and 22 % in the Clements et al., 1988, 1993), the acquisition of food is of Skagerrak off Sweden (Skôld et al., 1994 ), 59 % in major importance. The arms of crinoids (Meyer, 1982), Amphiura chiajei from Kilary Harbor (Munday, 1993), and asteroids (Jangoux, 1982), and ophiuroids (Warner, 1982) 11 % in intertidal and 6.4 % in subtidal populations of and the tentacles of holothuroids (Massin, 1982) are used Acrocnida brachiata in Douarnenez Bay, Brittany (Bour­ in feeding, and their loss by sublethal predation should goin and Guillou, 1994). This would require considerable decrease the ability to feed. The loss of the dise of crinoids allocation of production to regeneration. and ophiuroids involves the loss of the digestive system and would eliminate the ability to obtain resources. Duineveld and Van Noort (1986) calculated the loss of arms by Amphiura filiformis in the southern North Sea to The trauma of arm loss can also decrease feeding behavior. be ca. 0.84 g wet weight.m-2.a-1• The proportion of total The feeding posture is not assumed initially after arm loss in the comatulid Cenometra bella (Smith et al., 1981 ). production allocated to regeneration by A. filiformis was Removal of arm tips reduces feeding in the asteroid Pisas­ estimated to be 16 % in Galway Bay (O'Connor et al., ter giganteus for months, possibly by affecting the neuro­ 1986) and 13% in Skagerrak (Skold, 1994). sensory apparatus (Harrold and Pearse, 1980). Singletary ( 1970) calculated regeneration of body parts The well-known withdrawal reflex of tentacles of dendro­ amounts to 14-19 % of total organic production of Amphiu­ chirotid holothuroids indicates the probability of sublethal ra coniortodes, Ophionepthys limicola, and Microphiopho­ predation. The tentacles of the dendrochirotid holothuroids lis gracillima. These resources would not be available for Athyonidium chilensis at Playae el France s. Chile (V as­ growth or reproduction, and Singletary ( 1980) found a sug­ quez, unpub. obs.) and Eupentacta fraudatrix in Peter the gestive negative correlation between the amount of arm Great Bay, Russia (V. Levin, unpub. obs.) are preyed upon. loss and gonadal development for O. limicola. We know of no study on the effect of tentacle loss on fee­ The asteroid Luidia clathrata on a maintenance diet allo­ ding in holothuroids. cates few resources to regeneration (Lawrence et al., 1986) Ophiuroid behavior is affected by arm loss in ways that while the ophiuroid Microphiopholis gracillima regene­ should reduce feeding. Sediment-probing and arm-waving rates both the dise and arms even when starved (Fielman et activity by the arms is reduced in Microphiopholis gracilli­ al., 1991). Salzwedel (1974) reported at least sorne of the ma with lost arms and/or dise (Clements, 1985). The burro­ material for arm regeneration is derived from the dise in wing Acrocnida brachiata (Bourgoin, 1987) and Ophiop­ Amphiura filiformis. sila riisei (Grober, 1988 a) tend to keep their regenerating Regeneration in the field can be quite variable. Regenera­ arms below the surface and not use them for feeding. tion of the visceral mass by the crinoid Himerometra robustipinna was completed in sorne individuals by nine days while it was still incomplete in others after 23 days Effect on survivorship (Meyer, 1988). The basis for this difference in these indivi­ The effect of sublethal predation on survivorship is rarely duals that depend on reserves or dissolved organic material considered. The effects of attacks by the predatory shrimp is difficult to understand.

435 J. M. LAWRENCE, J. VASQUEZ

Remarkable control of allocation is indicated as allocation Correlation between effects of sublethal predation and of stored resources were allocated to the dise and/or arm life-history strategies regeneration until a gut and three complete arms were regenerated by Microphiopholis gracillima (Fielman et al., A basic tenet of life-history theory is that a suite of adap­ 1991 ). This is a remarkable parallel of the initial ontogene­ tive characteristics have evolved to environmental condi­ tic production of three long and two short arms in Ophio­ tions. According to Grime' s ( 1979) triangular model, spe­ phragmus filograneus (Turner, 197 4) and Amphiura filifor­ cies are adapted to combinations of stress (conditions that mis (Muus, 1981). Salzwedel (1974) did not find this decrease production) and disturbance (conditions that differentiai allocation to only a few arms in A. filiformis. decrease biomass). Species that are adapted to high levels He did report that the regenerating arms are intially thin, of disturbance such as sublethal predation must have low which he interpreted as a means to produce a functional, 1evels of stress. Lawrence ( 1991) noted this in comparing feeding arm with the investment of as few resources and in the asteroids Pisaster ochraceus, Asterias forbesi, and as short a period of ti me as possible. Asterias rubens. The former species may be a stress­ adapted species as it is food limited and almost never Rates of development in pentactula larvae of Eupentacta shows regeneration, while the latter two species may be fraudatrix decrease in individuals regenerating tentacles. disturbance-adapted species as they seem Jess food limit­ This could be a trade-off in allocation of resources even if ed and frequently show regeneration (see Lawrence, feeding is decreased. 1992). Whether regeneration results in an increase in total produc­ This concept is implicit in the suggestions that species with tion and in energy requirements is an intriguing question. different degrees of sublethal predation differ in their rates Mead ( 1901) concluded the Joss of two arms by Asterias of regeneration. Swan ( 1966) noted ophiuroids vary in the forbesi did not decrease the rate of growth. A direct corre­ lation between total production in arm regeneration with incidence of arm regeneration and that it is not known whether this is related to their ability to regenerate orto the the amount of arm loss in crinoids and ophiuroids (Salzwe­ del, 1974; Singletary, 1980; Mladenov, 1980, 1983; Bour­ frequency of encountering events causing arm loss. Litvi­ nova and Zharkov ( 1977) found Amphipholis kochii, which goin, 1987; Fielman et al., 1991; Clements et al., 1994; has a high incidence of sublethal predation, has a higher Stancyk et al., 1994) indicates a controlled increase. Pro­ capacity for regeneration than Ophiura sarsi, which does duction by Luidia clathrata fed below maintenance requi­ not. Lares and Lawrence (1994) similarly found a lower rements was by the gonads and pyloric caeca (Lawrence et al., 1986), while production by individuals fed above capacity for regeneration in the asteroid Echinaster paucis­ maintenance requirements was by both the viscera and the pina, which rarely shows arm -loss, than Luidia clathrata, which frequently shows arm Joss. bodywall (Lawrence and Ellwood, 1991). Production was greater in individuals with arm Joss than in those with As sublethal predation has an effect on the biology of intact arms (Lawrence and Ellwood, 1991 ). The greatl y echinoderms by affecting feeding and allocation of reduced amount of biomass, lipid, and energy in the pylo­ nutrients to growth and reproduction, does it have an ric caeca of the asteroid Stichaster striatus with regenera­ effect on their ecology and evolution ? Sublethal preda­ ting arms suggests a reduced capacity for feeding that tion is common in severa! marine invertebrate taxa and could affect capacity for reproduction (Lawrence and Lar­ has been considered an evolutionary factor (Vermeij, rain, 1994). 1982, 1987). Crawley (1983) pointed out that traditional If an increase in production follows sublethal predation, it animal population dynamics usually assumes change in must be associated with an increase in resource acquisition numbers alone is an adequate description of population or use of existing biomass and an increase in the rate of behavior, while changes in size and functioning must be respiration would be expected. Initial increases in oxygen included with the study of plants. Most models of popula­ consumption and production in the visceral mass was tion dynamics of animais assume lethal predation (Wil­ found after eviscerating the crinoid Cenometra bella bur, 1988; Kooijman, 1993). Harris (1989) proposed (Smith et al., 1981) and initial increases in oxygen sublethal predation is an important factor in the regula­ consumption and nitrogen excretion were found after tion of population size providing the criteria of density­ amputating arms from the ophiuroid Ophiocoma echinata dependency and depression of long-term survival and (Sullivan, 1988). Similarly, the respiration rate per unit reproduction are met. Viviani ( 1987) suggested sublethal weight of Ophiocoma echinata regenerating arms was predation on asteroids on the northern Chilean coast had much greater than that of non-regenerating individuals a great effect on their populations. (C. Pomory, unpubl. obs.). In contrast, no major change in Sublethal predation has been little considered in marine the rate of oxygen consumption was found after amputa­ communities that have focused on lethal predation. Aste­ ting arms from the ophiuroid microphiopholis gracillima roids are often major factors determining community (Golde, 1991 ), and the rates of oxygen consumption and structure (Paine 1971, 1974; Menge, 1982; Paine et al., nitrogen excretion were the same for the asteroid Luidia 1985; Menge and Farrell, 1989). Menge and Sutherland clathrata with regenerating or ail intact arms (Adams, ( 1987) proposed a mode! for community structure th at 1991 ). It is probable that the metabolism of regenerating depends directly on abiotic disturbance, competition and individuals depends on many variables, such as the physio­ lethal predation; and indirectly on recruitment and envi­ logical state of the individuals and resource availability. ronmental stress. The mode! does not consider an effect of Productionlbiomass and respirationlbiomass ratios change sublethal predation on recruitment or the ability to withs­ with size, nutritional state, and reproductive state. tand environmental stress. Sublethal predation can affect a

436 SUBLETHAL PREDATION IN ECHINODERMS species' behavior, morphology and physiology and thus Acknowledgements have an indirect effect on prey (Strauss, 1991 ). The biolo­ gie al importance of sublethal predation thus extends upwards from the organism to the population and commu­ We thank Michael Lares and Christopher Pomory for their nity and warrants attention. comments on a draft of this paper.

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