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Is there a latitudinal diversity cline in the sea?
TREE vol. 7, no. 9, September
In his long career, which ended earlier this year with his death at the age of 90, Imanishi’s thinking developed through different stages, becoming explicitly antidarwinian and culminating in an expression of ‘antiscience’. Both Ito and Halstead13 assume that lmanishi was simply removing himself from scientific debate by declaring himself no longer to be an ecologist, nor, later, a scientist. However, lmanishi perhaps meant something more profound”: that is, that a narrow selection of evidence in science is the chief impediment to the construction of a holistic world view. In speaking as a nonscientist, lmanishi attempted to make the intelligent layman conscious of the pitfalls of specialization and the constrictive natures of science, religion and other aspects of society that have broken the wholeness of our experience. ltb4 begins
his paper and ends with reference to Asian perspectives on science, and finds the basis for
Imanishi’s ideas in an Eastern, holistic philosophy. Although It6 repeatedly appears to gauge the value of developments within Japan by how far they anticipated developments in Western ecology, he concludes by stating that a ‘universal science’, a synergism of Western and Eastern insights, is desirable. Indeed, some Western thinkers” are already finding conceptual resources for environmental philosophy and ecology from Asian thought. References 1 Imanishi, K. (1938) Annot. Zoo/. Jpn 17, 23-36 2 Imanishi, K. (1941) Mem. Co//. SC;. Univ. Kyoto Ser. B 16, l-35 3 Imanishi, K. (1941) Seibutsu no Sekai [The World of Livina Thinasl. Koronsha 4 Ito, Y. (1991) Eco; Res. 6, ?39-155 5 Hiratsuka, E. (1920) Bull. Imp. Seric. Exp. Sta. 1,257-315 6 Imanishi, K. (1957) Shizen [Nature] 12, l-9 (in Japanese) 7 Sibatani, A. (1983) Riv. Biol. 76, 25-42 8 Asquith, P.J. (1991) in The Monkeys of
Is therea LatitudinalDiversity Clinein the Sea? Andrew
Clarke A CLINE IN THE SPECIES RICHNESS of terrestrial plants’ and animals’ from the tropics to the polar regions has long been recognized. However, the underlying reasons for this pattern are still not fully understood. Indeed, this has been called ‘the great unexplained feature of natural history’ (R. Ricklefs, quoted in Ref. 3). Despite the recent surge of interest in biodiversity, which has meant that this topic has once again received attention4-6, we remain in the position of being able to describe the phenomenon, but not explain it. It is usually assumed, and commonly reported in textbooks and popular articles, that a similar latitudinal cline in species richness is to be found in the sea. However, recent work on the deep sea and polar regions has indicated that this needs to be examined assumption critically. Andrew Clarke is at the British Survey, Cambridge, UK CB3 OET.
286
Antarctic
The first explicit demonstration of variation in marine species richness with latitude was that of Thorson’, who showed that there was a pronounced increase in the species richness of hard-substratum epifauna towards the tropics, but that in soft bottoms the number of infauna1 species was roughly the same for arctic, temperate and tropical regions. Since then, the clearest description of a latitudinal diversity cline in the sea has been that of Stehli et a/.*, who examined the diversity of bivalve molluscs at the species, genus and family level, pooled by 5” classes of latitude; the result was a distinct cline in diversity from the tropics toward both poles, with a clear centre of diversity in the Indo-West Pacific. The data for the northern hemisphere were more complete than for the southern hemisphere, and the Antarctic was represented by only a single point. Molluscs, however, are wellknown taxonomically and although recent systematic work in the
7992
Arashiyama: Thirty-five Years of Research in Japan and the West (Fedigan, L.M. and Asquith, P.J., eds), pp. 81-98. State University of New York Press 9 Asauith. P.J. (1986) in Primate Ontogenyand Behaviour(Else, J.G. and Lee, P.C., eds), pp. 61-71, Cambridge University Press 10 Asquith, P.J. (1986) Nature323, 675-676 11 Allee, W.C. (1938) Social Life of Animals, Norton 12 Ito, Y. (1980) Comparative Ecology, Cambridge University Press [lst Japanese edition, publ. 19591 13 Halstead, 6. (1985) Nature317. 587-589 14 Halstead, 6. (1987) Nature326,21 15 Sibatani, A. (1983) J. Social Biol. Struct. 6, 335-343 16 Kani, T. (1981) Physiol. Ecol. Japan 18, 113-118 (First published in Japanese in 1944) 17 Hokkyo, N. (1987) J. Social Biol. Struct. 10,377-379 18 Callicott, J.B. and Ames, R.T., eds (1989) Nature in Asian Traditions of Thought: Essays in Environmental Philosophy, State University of New York Press
Weddell Sea has added new taxag, it is unlikely that further work on the Southern Ocean molluscan fauna will alter the pattern significantly. Together with an earlier study of marine gastropods” and a later study of planktonic foraminifera”, these works comprise almost all of the basis for the assumption that there is a universal latitudinal diversity cline in the sea. Nevertheless, the trend in shallow-water marine molluscan biodiversity has been firmly established by generations of taxonomists, and factors such as biased sampling cannot be invoked to counter it. The question is: how general in the sea is the pattern established for molluscs and forams? One of the most difficult problems for studies of marine biodiversity is In that of standardizing techniques. making comparisons between different habitats or areas we must be
sure that we are measuring precisely the same thing at each place. Thus, the classic early work from the Marine Biological Laboratory at Woods Hole, which established the high diversity of the deep sea” and suggested a latitudinal difference in that diversity, suffers from the disadvantage that gear with differing sampling characteristics was used at the various sites. 0
1992, Elsev~er Sctence Publ,shers
Ltd (UK1
t
TREE vol. 7, no. 9, September
1992
Although some of these problems should be relatively easily solved, for instance by ensuring that comparable gear, sampling protocols 2nd computational techniques are used, there are other less tractable difficulties. The first is to decide precisely what is to be measured and compared: is it within-habitat (a), between-habitat CD) or regional (y) diversity that is to be considered? As an example, a detailed study of the fish fauna of the Weddell Sea has shown that the diversity of a typical sample is similar to that of an equivalent sample from the North Sea, and yet the regional diversity of the Weddell Sea, as a ivhole, is much lower than that of the North Sea13. The problem of choosing the appropriate scale is not simple, given the all-pervasive influence of scale and heterogeneity in marine biology. A comparison of the diversity of benthic foraminifera from 10 m to 5000 m depth indicated that the deep sea was speciesrich14; this has recently been confirmed in an exceptionally careful and detailed study of the fauna from ihe continental slope of eastern IJSA’. Although the high species richness of the deep sea has frequently invited comparison with coral reefs or tropical rain forests, it must be recognized that the size of ‘he organisms involved and the scale of heterogeneity in these three lnabitats are vastly different - so mnuch so that meaningful comparison may simply not be possible. So, what can we say about pres‘snt knowledge of diversity in the sea in relation to latitude? One interNesting feature is those taxa that iave been shown to exhibit a clear atitudinal diversity cline all have a :alcareous skeleton. Since the cost of calcification varies with temperature”, it is pertinent to ask whether non-calcareous taxa show the same zlines. Unfortunately, we simply do not have the data to judge. However, there are several groups of organisms that have been shown to be particularly species-rich in the Southern Ocean. These include sponges, bryozoans, polychaetes and amphipods (see Ref. 16 for discussion and original references). This would suggest the possibility (but no more) that not all marine taxa show a latitudinal cline in diversity. We are also reassessing our view of the diversity of polar regions, and particularly the Southern Ocean. For many years the polar seas have been regarded as poor in species, and essentially the passive recipient
of taxa that originated elsewhere. This is partly because many early studies were confined (for logistic reasons) to the Arctic, which in many areas is genuinely depauperate, being in the process of recovery from recent intense glaciation17. Recent work on the fossil record of marine faunas around Gondwana, however, has shown that the continental shelves around what is now Antarctica have a long history of fauna1 diversification and colonization, which is probably still continuing 16,“. It is possible that recent climatic cycles have acted as a diversity pump, concentrating taxa in high latitudes18, and that frequent fragmentation and recombination of the distribution of shallow water marine invertebrates, due to the advance and retreat of continental ice shelves, may also have promoted speciation 16. Further systematic work is badly needed, but these recent developments in our knowledge of polar faunas indicate that it is premature to assume a widespread latitudinal cline in the diversity of all marine taxa. The data for molluscan diversity collated by Stehli et al.” approximate to regional diversity, for they pool all known species within a given range of latitudes, regardless of habitat or location. This is fine for molluscs, but given our poor taxonomic knowledge of many marine invertebrate groups, an alternative approach for establishing the possibility of a latitudinal diversity cline is required. One such method is to look at within-habitat diversity for a variety of sites from different latitudes. Data for soft-bottom communities were examined some years ago by Richardson and Hedgpethlg. These data inevitably suffer from the difficulties of comparison outlined above, particularly because the authors were forced to combine data from estuaries, shallow continental shelves and deep continental shelves and the range of latitudes covered is rather narrow. However, they are still the best data openly available for comparison and they do not suggest a latitudinal cline in the within-habitat diversity of soft-bottom communities, which was also the original conclusion of Thorson7. So, what is the answer to the question posed in the title? It must be that for soft substrata withinhabitat diversity seems to be high, especially in the deep sea, but there is no convincing evidence for a latitudinal cline. For some taxa there is clear evidence of a cline (for
example gastropods, bivalves and foraminifera); for others the evidence is equivocal, with the possibility of high species richness in the Southern Ocean. Overall we must conclude that, as yet, there is no convincing evidence of a latitudinal cline across all taxa comparable with that seen on land. With the need for data on diversity becoming ever more urgent for both academic and conservation reasons, this emphasizes the need for continued work in those areas currently unfashionable with funding agencies: systematics, biogeography and taxonomy. Perhaps we have come full circle, and are once again realizing the contribution that such basic studies can make to our understanding of the big biological problems. References 1 Woodward, F.I. (1987) Climate and Cambridge Planr Distribution, University Press 2 Pianka, E.R. (1966) Am. Nat. 100, 33-46 3 Lewin, R. (1989) Science 244,527-528 4 France, R. (1992) Am. Nat. 193, 342-354 5 Stevens, G.C. (1989) Am. Nat. 133, 240-256 6 Grassle, J.F. and Maciolek, N.J. (1992) Am. Nat. 139.313-341 7 Thorson, G. (1957) in Treatise on Marine Ecology and Palaeoecology
(Hedgpeth, J.W., ed.), pp. 461-534, Geological Society of America 8 Stehli, F.G., McAlester, A.L. and Helsley, C.E. (1967) Bull. Geol. Sot. Am. 78, 455-466 9 Hain, S. (1990) Ber. Polarforsch. 70, 181 10 Fischer, A.G. (1960) Evolution 14, 64-81 11 Stehli, F.G., Douglas, R. and Kafescegliou, I. (1972) in Mode/s for the Evolution of Planktonic Foraminifera (Schopf, T.J.M., ed.), pp. 116-128, Freeman 12 Sanders, H.L. (1968) Am. Nat. 102, 243-282 13 Hubold, G. (1992) Ber. Polarforsch. 103,157 14 Buzas, M.A. and Gibson, T.G. (1969) Science 163,72-75 15 Clarke, A. (1983) Oceanogr. Mar. EGO/.21, 341-453 16 Clarke, A. and Crame, J.A. (1989) in Origins and Evolution of the Antarctic Rota (Crame, J.A., ed.), pp. 253-268, Cambridge University Press 17 Dunton, K. (1992) Trends Ecol. Evol. 7, 183-189 18 Crame, J.A. (1992) IIist. Biol. 6, 37-60 19 Richardson, M.D. and Hedgpeth, J.W. (1977) in Adaptations Within Antarctic Ecosystems (Llano, G.A., ed.), pp. 181-196, The Smithsonian Institution
287
In his long career, which ended earlier this year with his death at the age of 90, Imanishi’s thinking developed through different stages, becoming explicitly antidarwinian and culminating in an expression of ‘antiscience’. Both Ito and Halstead13 assume that lmanishi was simply removing himself from scientific debate by declaring himself no longer to be an ecologist, nor, later, a scientist. However, lmanishi perhaps meant something more profound”: that is, that a narrow selection of evidence in science is the chief impediment to the construction of a holistic world view. In speaking as a nonscientist, lmanishi attempted to make the intelligent layman conscious of the pitfalls of specialization and the constrictive natures of science, religion and other aspects of society that have broken the wholeness of our experience. ltb4 begins
his paper and ends with reference to Asian perspectives on science, and finds the basis for
Imanishi’s ideas in an Eastern, holistic philosophy. Although It6 repeatedly appears to gauge the value of developments within Japan by how far they anticipated developments in Western ecology, he concludes by stating that a ‘universal science’, a synergism of Western and Eastern insights, is desirable. Indeed, some Western thinkers” are already finding conceptual resources for environmental philosophy and ecology from Asian thought. References 1 Imanishi, K. (1938) Annot. Zoo/. Jpn 17, 23-36 2 Imanishi, K. (1941) Mem. Co//. SC;. Univ. Kyoto Ser. B 16, l-35 3 Imanishi, K. (1941) Seibutsu no Sekai [The World of Livina Thinasl. Koronsha 4 Ito, Y. (1991) Eco; Res. 6, ?39-155 5 Hiratsuka, E. (1920) Bull. Imp. Seric. Exp. Sta. 1,257-315 6 Imanishi, K. (1957) Shizen [Nature] 12, l-9 (in Japanese) 7 Sibatani, A. (1983) Riv. Biol. 76, 25-42 8 Asquith, P.J. (1991) in The Monkeys of
Is therea LatitudinalDiversity Clinein the Sea? Andrew
Clarke A CLINE IN THE SPECIES RICHNESS of terrestrial plants’ and animals’ from the tropics to the polar regions has long been recognized. However, the underlying reasons for this pattern are still not fully understood. Indeed, this has been called ‘the great unexplained feature of natural history’ (R. Ricklefs, quoted in Ref. 3). Despite the recent surge of interest in biodiversity, which has meant that this topic has once again received attention4-6, we remain in the position of being able to describe the phenomenon, but not explain it. It is usually assumed, and commonly reported in textbooks and popular articles, that a similar latitudinal cline in species richness is to be found in the sea. However, recent work on the deep sea and polar regions has indicated that this needs to be examined assumption critically. Andrew Clarke is at the British Survey, Cambridge, UK CB3 OET.
286
Antarctic
The first explicit demonstration of variation in marine species richness with latitude was that of Thorson’, who showed that there was a pronounced increase in the species richness of hard-substratum epifauna towards the tropics, but that in soft bottoms the number of infauna1 species was roughly the same for arctic, temperate and tropical regions. Since then, the clearest description of a latitudinal diversity cline in the sea has been that of Stehli et a/.*, who examined the diversity of bivalve molluscs at the species, genus and family level, pooled by 5” classes of latitude; the result was a distinct cline in diversity from the tropics toward both poles, with a clear centre of diversity in the Indo-West Pacific. The data for the northern hemisphere were more complete than for the southern hemisphere, and the Antarctic was represented by only a single point. Molluscs, however, are wellknown taxonomically and although recent systematic work in the
7992
Arashiyama: Thirty-five Years of Research in Japan and the West (Fedigan, L.M. and Asquith, P.J., eds), pp. 81-98. State University of New York Press 9 Asauith. P.J. (1986) in Primate Ontogenyand Behaviour(Else, J.G. and Lee, P.C., eds), pp. 61-71, Cambridge University Press 10 Asquith, P.J. (1986) Nature323, 675-676 11 Allee, W.C. (1938) Social Life of Animals, Norton 12 Ito, Y. (1980) Comparative Ecology, Cambridge University Press [lst Japanese edition, publ. 19591 13 Halstead, 6. (1985) Nature317. 587-589 14 Halstead, 6. (1987) Nature326,21 15 Sibatani, A. (1983) J. Social Biol. Struct. 6, 335-343 16 Kani, T. (1981) Physiol. Ecol. Japan 18, 113-118 (First published in Japanese in 1944) 17 Hokkyo, N. (1987) J. Social Biol. Struct. 10,377-379 18 Callicott, J.B. and Ames, R.T., eds (1989) Nature in Asian Traditions of Thought: Essays in Environmental Philosophy, State University of New York Press
Weddell Sea has added new taxag, it is unlikely that further work on the Southern Ocean molluscan fauna will alter the pattern significantly. Together with an earlier study of marine gastropods” and a later study of planktonic foraminifera”, these works comprise almost all of the basis for the assumption that there is a universal latitudinal diversity cline in the sea. Nevertheless, the trend in shallow-water marine molluscan biodiversity has been firmly established by generations of taxonomists, and factors such as biased sampling cannot be invoked to counter it. The question is: how general in the sea is the pattern established for molluscs and forams? One of the most difficult problems for studies of marine biodiversity is In that of standardizing techniques. making comparisons between different habitats or areas we must be
sure that we are measuring precisely the same thing at each place. Thus, the classic early work from the Marine Biological Laboratory at Woods Hole, which established the high diversity of the deep sea” and suggested a latitudinal difference in that diversity, suffers from the disadvantage that gear with differing sampling characteristics was used at the various sites. 0
1992, Elsev~er Sctence Publ,shers
Ltd (UK1
t
TREE vol. 7, no. 9, September
1992
Although some of these problems should be relatively easily solved, for instance by ensuring that comparable gear, sampling protocols 2nd computational techniques are used, there are other less tractable difficulties. The first is to decide precisely what is to be measured and compared: is it within-habitat (a), between-habitat CD) or regional (y) diversity that is to be considered? As an example, a detailed study of the fish fauna of the Weddell Sea has shown that the diversity of a typical sample is similar to that of an equivalent sample from the North Sea, and yet the regional diversity of the Weddell Sea, as a ivhole, is much lower than that of the North Sea13. The problem of choosing the appropriate scale is not simple, given the all-pervasive influence of scale and heterogeneity in marine biology. A comparison of the diversity of benthic foraminifera from 10 m to 5000 m depth indicated that the deep sea was speciesrich14; this has recently been confirmed in an exceptionally careful and detailed study of the fauna from ihe continental slope of eastern IJSA’. Although the high species richness of the deep sea has frequently invited comparison with coral reefs or tropical rain forests, it must be recognized that the size of ‘he organisms involved and the scale of heterogeneity in these three lnabitats are vastly different - so mnuch so that meaningful comparison may simply not be possible. So, what can we say about pres‘snt knowledge of diversity in the sea in relation to latitude? One interNesting feature is those taxa that iave been shown to exhibit a clear atitudinal diversity cline all have a :alcareous skeleton. Since the cost of calcification varies with temperature”, it is pertinent to ask whether non-calcareous taxa show the same zlines. Unfortunately, we simply do not have the data to judge. However, there are several groups of organisms that have been shown to be particularly species-rich in the Southern Ocean. These include sponges, bryozoans, polychaetes and amphipods (see Ref. 16 for discussion and original references). This would suggest the possibility (but no more) that not all marine taxa show a latitudinal cline in diversity. We are also reassessing our view of the diversity of polar regions, and particularly the Southern Ocean. For many years the polar seas have been regarded as poor in species, and essentially the passive recipient
of taxa that originated elsewhere. This is partly because many early studies were confined (for logistic reasons) to the Arctic, which in many areas is genuinely depauperate, being in the process of recovery from recent intense glaciation17. Recent work on the fossil record of marine faunas around Gondwana, however, has shown that the continental shelves around what is now Antarctica have a long history of fauna1 diversification and colonization, which is probably still continuing 16,“. It is possible that recent climatic cycles have acted as a diversity pump, concentrating taxa in high latitudes18, and that frequent fragmentation and recombination of the distribution of shallow water marine invertebrates, due to the advance and retreat of continental ice shelves, may also have promoted speciation 16. Further systematic work is badly needed, but these recent developments in our knowledge of polar faunas indicate that it is premature to assume a widespread latitudinal cline in the diversity of all marine taxa. The data for molluscan diversity collated by Stehli et al.” approximate to regional diversity, for they pool all known species within a given range of latitudes, regardless of habitat or location. This is fine for molluscs, but given our poor taxonomic knowledge of many marine invertebrate groups, an alternative approach for establishing the possibility of a latitudinal diversity cline is required. One such method is to look at within-habitat diversity for a variety of sites from different latitudes. Data for soft-bottom communities were examined some years ago by Richardson and Hedgpethlg. These data inevitably suffer from the difficulties of comparison outlined above, particularly because the authors were forced to combine data from estuaries, shallow continental shelves and deep continental shelves and the range of latitudes covered is rather narrow. However, they are still the best data openly available for comparison and they do not suggest a latitudinal cline in the within-habitat diversity of soft-bottom communities, which was also the original conclusion of Thorson7. So, what is the answer to the question posed in the title? It must be that for soft substrata withinhabitat diversity seems to be high, especially in the deep sea, but there is no convincing evidence for a latitudinal cline. For some taxa there is clear evidence of a cline (for
example gastropods, bivalves and foraminifera); for others the evidence is equivocal, with the possibility of high species richness in the Southern Ocean. Overall we must conclude that, as yet, there is no convincing evidence of a latitudinal cline across all taxa comparable with that seen on land. With the need for data on diversity becoming ever more urgent for both academic and conservation reasons, this emphasizes the need for continued work in those areas currently unfashionable with funding agencies: systematics, biogeography and taxonomy. Perhaps we have come full circle, and are once again realizing the contribution that such basic studies can make to our understanding of the big biological problems. References 1 Woodward, F.I. (1987) Climate and Cambridge Planr Distribution, University Press 2 Pianka, E.R. (1966) Am. Nat. 100, 33-46 3 Lewin, R. (1989) Science 244,527-528 4 France, R. (1992) Am. Nat. 193, 342-354 5 Stevens, G.C. (1989) Am. Nat. 133, 240-256 6 Grassle, J.F. and Maciolek, N.J. (1992) Am. Nat. 139.313-341 7 Thorson, G. (1957) in Treatise on Marine Ecology and Palaeoecology
(Hedgpeth, J.W., ed.), pp. 461-534, Geological Society of America 8 Stehli, F.G., McAlester, A.L. and Helsley, C.E. (1967) Bull. Geol. Sot. Am. 78, 455-466 9 Hain, S. (1990) Ber. Polarforsch. 70, 181 10 Fischer, A.G. (1960) Evolution 14, 64-81 11 Stehli, F.G., Douglas, R. and Kafescegliou, I. (1972) in Mode/s for the Evolution of Planktonic Foraminifera (Schopf, T.J.M., ed.), pp. 116-128, Freeman 12 Sanders, H.L. (1968) Am. Nat. 102, 243-282 13 Hubold, G. (1992) Ber. Polarforsch. 103,157 14 Buzas, M.A. and Gibson, T.G. (1969) Science 163,72-75 15 Clarke, A. (1983) Oceanogr. Mar. EGO/.21, 341-453 16 Clarke, A. and Crame, J.A. (1989) in Origins and Evolution of the Antarctic Rota (Crame, J.A., ed.), pp. 253-268, Cambridge University Press 17 Dunton, K. (1992) Trends Ecol. Evol. 7, 183-189 18 Crame, J.A. (1992) IIist. Biol. 6, 37-60 19 Richardson, M.D. and Hedgpeth, J.W. (1977) in Adaptations Within Antarctic Ecosystems (Llano, G.A., ed.), pp. 181-196, The Smithsonian Institution
287