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Unique spawning behaviour by the Antarctic limpet Nacella (Patinigera) concinna (Strebel, 1908)
J. Exp. Mar. Biol. Ecol., 1983, Vol. 71, pp. 283-287
283
Elsevier
UNIQUE SPAWNING
NACELLA
BEHAVIOUR
(PATINIGERA)
GORDON
BY THE ANTARCTIC
CONCINNA
B. PICKEN’
LIMPET
(Strebel, 1908)
and DOUGLAS ALLAN
British Antarctic Survey. Natural Environment Research Council, High Cross, Madingfey Road, Cambridge, CB3 OET, England
The Antarctic limpet NaceNa (Putinigeru) concinna (Strebel, 1908) forms temporary “stacks” before spawning, a behaviour which ensures that gametes are released in close proximity. This promotes the fertilization of a large prounion of eggs, so reducing the energy outlay necessary to ensure reproductive success. The annual reproductive output of Nuceita is low in comparison with other Patelhdae. Rapid fertilization may also help to contain larvae in shallow coastal waters suitable for settlement. Evidence of this unique spawning behaviour has now been obtained in a series of photographs taken at Signy Island, South Orkney Islands (60” S : 43’ W). Abstract:
INTRODUCTION
Following preliminary observations on the spawning of the Antarctic limpet Nacella concinna (Picken, 1980a), we now present further observations and the first photographic evidence of this extraordinary adaptation. Although pairing before spawning has been reported in other Patellidae (Willcox, 1905; Ankel, 1936; von Medem, 1945>, the behaviour of the Antarctic limpet is unique, because mature adults form “stacks” immediately before spawning in the austral summer (December).
DESCRIPTION
OF THE BEHAVIOLIR
Nacella stacks consist of up to eight adults, each animal resting on the shell of the one beneath. All the individuals hold their bodies in an extremely extended position, and maintain this attitude while eggs and sperm are released (Figs. 1 and 2). Animals are not arranged in alternating order of sexes, nor do the stacks necessarily contain equal numbers of males and females. As well as forming well-defmed stacks, adults may cluster over and around each other in unnatural aggregations. Stacking is not an artefact of overcrowding because there is ample unoccupied suitable substratum nearby (Fig. 2); it is a deliberate behaviour, seen only at spawning. Spawning is synchronous among adults over small areas in the shallow sublittoral (6 m depth) and, ~~0~ the duration of stacking is unknown, it does not last longer than 24 h at any one site. Water temperature is an important factor in the final ’ Present address: Department of Zoology, University of Aberdeen, Aberdeen, AB92TN, Scotland. 0022-0981/83/$03.00 0 1983 Elsevier Science Publishers B.V.
284
GORDON B. PICKEN AND DOUGLAS ALLAN
maturation of Nucellu gonads (Shabica, 1971), and our observations support the view that spawning occurs 3-4 wk after temperature in the shallow sublittoral has risen above - 1.4 “C. In four Decembers (1975, 1976, 1979, 1980), spawning has been recorded 22,26,29, and 30 days, respectively after this temperature was exceeded. At the sites in question no other spawning was observed at any time prior to or following the observed behaviour. Clearly, a more precise mechanism triggers localized stacking behaviour once final gonad maturation is achieved. A pheromone is the most likely agent, as pheromones are known to synchronize spawning in abalones (Morse et al., 1977).
Fig. 1. Spawning stacks of the Antarctic limpet Nacella (Patinigera) concinna, at Signy Island, South Orkney Islands: stacks consisting of up to eight adults form in late December-early January, after the temperature of water in the shallow sublittoral (6 m depth) has increased z - 1.4 “C; the synchronous release of sperm and eggs (stream of pale dots in the upper left corner) is clearly seen; the main stack consists of five animals with a “side branch” of two; photograph by Douglas Allan.
Stacks are probably formed by the passive addition of individuals at the bottom. A limpet bearing one or more adults on its shell climbs onto the shell of another, while the stacked individuals maintain their positions. Alternatively, new animals may join actively by climbing up the sides of animals already in the stack. This may be a less likely method, since it would be more time-consuming and render incipient stacks
UNlQUESPAWNINGOETHEANTARCTICLIMPET
285
unstable. From the photographic evidence obtained, no specific conclusion can be made but, whatever the method, there must be some advantage to such a laborious activity. The most obvious likely benefit is an increase in the success of fixation.
Fig. 2. Spawning stacks ofthe Antarctic limpet Nacella (Patinigera) concinna, at Signy Island, South Orkney Islands: animals in the stack are usually in the size range 25-35 mm long, and hold their bodies in an extremely extended posture during spawning; an isolated stack of six animals, with ample unoccupied substratum around it, shows that stacking is not an artefact of overcrowding; photograph by Douglas Allan.
DISCUSSION
There is a predominance of non-pelagic development among Antarctic benthic invertebrates which is probably the result of environmental constraints imposed by low temperatures and the short summer period of primary production (Thorson, 1950; Picken, 1980b). In environments where food is scarce, or its availability seasonal but predictable, it is theoretically more efficient to invest energy in a small number of yolk-rich eggs that develop non-pelagically, than in numerous yolk-deficient eggs that develop pl~kto~op~c~y (Vance, 1973). The reproductive adaptations of Antarctic gastropods conform with this analysis. With the exception of A&e&z, all the Antarctic prosobranchs so far studi’ed develop non-pelagically (Picken, 1979). Nucella has not
286
GORDON B. PICKEN AND DOUGLAS ALLAN
adapted to the same extent as the boreal Acmaea rubella (Thorson, 1935) or members of the genus Problacmea (Golikov & Kussakin, 1972; Lindberg, 1979) which brood their young, but it does have a low reproductive effort in comparison with other limpets. Various Patella species have reproductive outputs ranging from 9-92 % of their somatic weight (Branch, 1981); female Nacella have a reproductive output of x 12% of their somatic weight (Picken, 1980a). Stacking may help to keep the output low by increasing fertilization success. From known ecological factors, the reproductive output of Nacella might be expected to be low. In the sublittoral at least, the environment is stable, adults grow slowly, are longevious and probably reproduce several times in their life. It is also very likely that recruitment to the population sometimes fails catastrophically when larvae are transported out to sea and settle in unfavourable habitats. Although Nacella has been collected at depths of up to 110 m (Powell, 1973), greatest densities are found in the depth range 3-6 m on rocky substrata bearing macroalgae (Picken, 1980a). This habitat is largely confined to islands in the Scotia Arc and the coast of the Antarctic Peninsula. The most vulnerable period for Nacella may, therefore, be before benthonic settlement, and if stacking hastens development to this stage, recruitment will be enhanced. A small annual reproductive output would also lessen the detrimental effects of occasional failures in recruitment. The full significance of stacking will be appreciated only when the larval form of Nacella is found and its development known in detail.
ACKNOWLEDGEMENTS
We thank our friends at Signy Island for help with boating and diving, and colleagues at B.A.S. Cambridge for their useful comments on the manuscript.
REFERENCES ANKEL, W.E., 1936. Prosobranchia. Tierwelt N. Ostsee, Vol. 29, pp. l-240. BRANCH,G. M., 1981. The biology of limpets: physical factors, energy flow, and ecological interactions. Oceanogr. Mar. Biol. Annu. Rev., Vol. 19, pp. 235-380. GOLIKOV,A.N. & O.G. KUSSAKIN, 1972. Sur la biologie de la reproduction des patelles de la famille Tecturidae (Gastropoda : Docoglossa) et sur la position systematique de ses subdivisions. Malacologia, Vol. 11, pp. 287-294. LINDBERG,D. R., 1979. Problacmaea moskalevi Golikov & Kussakin, a new addition to the eastern Pacific limpet fauna. Veliger, Vol. 22, pp. 57-60. MEDEM, F.G. VON, 1945. Untersuchungen iiber die Ei- und Spermawirkstoffe bei marinen Mollusken. Zool. Jb. Abt. Anat. Ontog. Tiere, Vol. 61, pp. l-44. MORSE, D.E., H. DUNCAN, N. HOOKER & A. MORSE, 1977. Hydrogen peroxide induces spawning in molluscs, with activation of prostaglandin endoperoxide synthetase. Science, Vol. 196, pp. 298-300. PICKEN, G.B., 1979. Non-pelagic reproduction of some Antarctic prosobranch gastropods from Signy Island, South Orkney Islands. Malacofogia, Vol. 19, pp. 109-128. PICKEN,G. B., 1980a. The distribution, growth and reproduction of the Antarctic limpet Naceila (Patinigera) con&ma (Strebel, 1908). J. Exp. Mar. Biol. Ecol., Vol. 42, pp. 71-85. PICKEN,G.B., 1980b. Reproductive adaptations of Antarctic benthic invertebrates. Biol. J. Linn. Sot., Vol. 14, pp. 67-75.
UNIQUE SPAWNING
OF THE ANTARCTIC
LIMPET
281
POWELL, A.W.B., 1973. The patellid limpets of the world (Patellidae). Indo-Pacific Mollusca, Vol. 3, pp. 75-206. SHABICA,S.V., 1971. The general ecology of the Antarctic limpet Patinigera polank Antarct. J. U.S., Vol. 6, pp. 160-162. THORSON,G., 1935. Studies on the egg capsules and development of Arctic marine prosobranchs. Medd. GrenL, Vol. 100, pp. 1-71. THORSON,G., 1950. Reproductive and larval ecology of marine bottom invertebrates. Biol. Rev., Vol. 25, pp. l-45. VANCE, R.R., 1973. On reproductive strategies in marine benthic invertebrates. Am. Nat., Vol. 107, pp. 339-352. WILLCOX,M.A., 1905. Biology of Acmaea testudinalis. Am. Nat., Vol. 39, pp. 325-333.
283
Elsevier
UNIQUE SPAWNING
NACELLA
BEHAVIOUR
(PATINIGERA)
GORDON
BY THE ANTARCTIC
CONCINNA
B. PICKEN’
LIMPET
(Strebel, 1908)
and DOUGLAS ALLAN
British Antarctic Survey. Natural Environment Research Council, High Cross, Madingfey Road, Cambridge, CB3 OET, England
The Antarctic limpet NaceNa (Putinigeru) concinna (Strebel, 1908) forms temporary “stacks” before spawning, a behaviour which ensures that gametes are released in close proximity. This promotes the fertilization of a large prounion of eggs, so reducing the energy outlay necessary to ensure reproductive success. The annual reproductive output of Nuceita is low in comparison with other Patelhdae. Rapid fertilization may also help to contain larvae in shallow coastal waters suitable for settlement. Evidence of this unique spawning behaviour has now been obtained in a series of photographs taken at Signy Island, South Orkney Islands (60” S : 43’ W). Abstract:
INTRODUCTION
Following preliminary observations on the spawning of the Antarctic limpet Nacella concinna (Picken, 1980a), we now present further observations and the first photographic evidence of this extraordinary adaptation. Although pairing before spawning has been reported in other Patellidae (Willcox, 1905; Ankel, 1936; von Medem, 1945>, the behaviour of the Antarctic limpet is unique, because mature adults form “stacks” immediately before spawning in the austral summer (December).
DESCRIPTION
OF THE BEHAVIOLIR
Nacella stacks consist of up to eight adults, each animal resting on the shell of the one beneath. All the individuals hold their bodies in an extremely extended position, and maintain this attitude while eggs and sperm are released (Figs. 1 and 2). Animals are not arranged in alternating order of sexes, nor do the stacks necessarily contain equal numbers of males and females. As well as forming well-defmed stacks, adults may cluster over and around each other in unnatural aggregations. Stacking is not an artefact of overcrowding because there is ample unoccupied suitable substratum nearby (Fig. 2); it is a deliberate behaviour, seen only at spawning. Spawning is synchronous among adults over small areas in the shallow sublittoral (6 m depth) and, ~~0~ the duration of stacking is unknown, it does not last longer than 24 h at any one site. Water temperature is an important factor in the final ’ Present address: Department of Zoology, University of Aberdeen, Aberdeen, AB92TN, Scotland. 0022-0981/83/$03.00 0 1983 Elsevier Science Publishers B.V.
284
GORDON B. PICKEN AND DOUGLAS ALLAN
maturation of Nucellu gonads (Shabica, 1971), and our observations support the view that spawning occurs 3-4 wk after temperature in the shallow sublittoral has risen above - 1.4 “C. In four Decembers (1975, 1976, 1979, 1980), spawning has been recorded 22,26,29, and 30 days, respectively after this temperature was exceeded. At the sites in question no other spawning was observed at any time prior to or following the observed behaviour. Clearly, a more precise mechanism triggers localized stacking behaviour once final gonad maturation is achieved. A pheromone is the most likely agent, as pheromones are known to synchronize spawning in abalones (Morse et al., 1977).
Fig. 1. Spawning stacks of the Antarctic limpet Nacella (Patinigera) concinna, at Signy Island, South Orkney Islands: stacks consisting of up to eight adults form in late December-early January, after the temperature of water in the shallow sublittoral (6 m depth) has increased z - 1.4 “C; the synchronous release of sperm and eggs (stream of pale dots in the upper left corner) is clearly seen; the main stack consists of five animals with a “side branch” of two; photograph by Douglas Allan.
Stacks are probably formed by the passive addition of individuals at the bottom. A limpet bearing one or more adults on its shell climbs onto the shell of another, while the stacked individuals maintain their positions. Alternatively, new animals may join actively by climbing up the sides of animals already in the stack. This may be a less likely method, since it would be more time-consuming and render incipient stacks
UNlQUESPAWNINGOETHEANTARCTICLIMPET
285
unstable. From the photographic evidence obtained, no specific conclusion can be made but, whatever the method, there must be some advantage to such a laborious activity. The most obvious likely benefit is an increase in the success of fixation.
Fig. 2. Spawning stacks ofthe Antarctic limpet Nacella (Patinigera) concinna, at Signy Island, South Orkney Islands: animals in the stack are usually in the size range 25-35 mm long, and hold their bodies in an extremely extended posture during spawning; an isolated stack of six animals, with ample unoccupied substratum around it, shows that stacking is not an artefact of overcrowding; photograph by Douglas Allan.
DISCUSSION
There is a predominance of non-pelagic development among Antarctic benthic invertebrates which is probably the result of environmental constraints imposed by low temperatures and the short summer period of primary production (Thorson, 1950; Picken, 1980b). In environments where food is scarce, or its availability seasonal but predictable, it is theoretically more efficient to invest energy in a small number of yolk-rich eggs that develop non-pelagically, than in numerous yolk-deficient eggs that develop pl~kto~op~c~y (Vance, 1973). The reproductive adaptations of Antarctic gastropods conform with this analysis. With the exception of A&e&z, all the Antarctic prosobranchs so far studi’ed develop non-pelagically (Picken, 1979). Nucella has not
286
GORDON B. PICKEN AND DOUGLAS ALLAN
adapted to the same extent as the boreal Acmaea rubella (Thorson, 1935) or members of the genus Problacmea (Golikov & Kussakin, 1972; Lindberg, 1979) which brood their young, but it does have a low reproductive effort in comparison with other limpets. Various Patella species have reproductive outputs ranging from 9-92 % of their somatic weight (Branch, 1981); female Nacella have a reproductive output of x 12% of their somatic weight (Picken, 1980a). Stacking may help to keep the output low by increasing fertilization success. From known ecological factors, the reproductive output of Nacella might be expected to be low. In the sublittoral at least, the environment is stable, adults grow slowly, are longevious and probably reproduce several times in their life. It is also very likely that recruitment to the population sometimes fails catastrophically when larvae are transported out to sea and settle in unfavourable habitats. Although Nacella has been collected at depths of up to 110 m (Powell, 1973), greatest densities are found in the depth range 3-6 m on rocky substrata bearing macroalgae (Picken, 1980a). This habitat is largely confined to islands in the Scotia Arc and the coast of the Antarctic Peninsula. The most vulnerable period for Nacella may, therefore, be before benthonic settlement, and if stacking hastens development to this stage, recruitment will be enhanced. A small annual reproductive output would also lessen the detrimental effects of occasional failures in recruitment. The full significance of stacking will be appreciated only when the larval form of Nacella is found and its development known in detail.
ACKNOWLEDGEMENTS
We thank our friends at Signy Island for help with boating and diving, and colleagues at B.A.S. Cambridge for their useful comments on the manuscript.
REFERENCES ANKEL, W.E., 1936. Prosobranchia. Tierwelt N. Ostsee, Vol. 29, pp. l-240. BRANCH,G. M., 1981. The biology of limpets: physical factors, energy flow, and ecological interactions. Oceanogr. Mar. Biol. Annu. Rev., Vol. 19, pp. 235-380. GOLIKOV,A.N. & O.G. KUSSAKIN, 1972. Sur la biologie de la reproduction des patelles de la famille Tecturidae (Gastropoda : Docoglossa) et sur la position systematique de ses subdivisions. Malacologia, Vol. 11, pp. 287-294. LINDBERG,D. R., 1979. Problacmaea moskalevi Golikov & Kussakin, a new addition to the eastern Pacific limpet fauna. Veliger, Vol. 22, pp. 57-60. MEDEM, F.G. VON, 1945. Untersuchungen iiber die Ei- und Spermawirkstoffe bei marinen Mollusken. Zool. Jb. Abt. Anat. Ontog. Tiere, Vol. 61, pp. l-44. MORSE, D.E., H. DUNCAN, N. HOOKER & A. MORSE, 1977. Hydrogen peroxide induces spawning in molluscs, with activation of prostaglandin endoperoxide synthetase. Science, Vol. 196, pp. 298-300. PICKEN, G.B., 1979. Non-pelagic reproduction of some Antarctic prosobranch gastropods from Signy Island, South Orkney Islands. Malacofogia, Vol. 19, pp. 109-128. PICKEN,G. B., 1980a. The distribution, growth and reproduction of the Antarctic limpet Naceila (Patinigera) con&ma (Strebel, 1908). J. Exp. Mar. Biol. Ecol., Vol. 42, pp. 71-85. PICKEN,G.B., 1980b. Reproductive adaptations of Antarctic benthic invertebrates. Biol. J. Linn. Sot., Vol. 14, pp. 67-75.
UNIQUE SPAWNING
OF THE ANTARCTIC
LIMPET
281
POWELL, A.W.B., 1973. The patellid limpets of the world (Patellidae). Indo-Pacific Mollusca, Vol. 3, pp. 75-206. SHABICA,S.V., 1971. The general ecology of the Antarctic limpet Patinigera polank Antarct. J. U.S., Vol. 6, pp. 160-162. THORSON,G., 1935. Studies on the egg capsules and development of Arctic marine prosobranchs. Medd. GrenL, Vol. 100, pp. 1-71. THORSON,G., 1950. Reproductive and larval ecology of marine bottom invertebrates. Biol. Rev., Vol. 25, pp. l-45. VANCE, R.R., 1973. On reproductive strategies in marine benthic invertebrates. Am. Nat., Vol. 107, pp. 339-352. WILLCOX,M.A., 1905. Biology of Acmaea testudinalis. Am. Nat., Vol. 39, pp. 325-333.