- Email: [email protected]
Culling predators to protect fisheries: a case of accumulating uncertainties
282
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interactions. Quite apart from the issues of external forcing of ecosystems, the requirements for large volumes of temporally relevant and expensively obtained data might ultimately rule out the multispecies approach as a practical solution. Finally, perhaps the justification for or against culling predators as a form of fisheries management has greater dimensionality than even the complex food web models described by Yodzis. Since before Horace considered the conflicting paradigms of use and delight for his garden in the 1st Century BC (Ref. 14), people have battled with the difficult balance of utilitarianism versus aestheticism. For a variety of reasons, marine predators currently appeal more for aesthetic reasons than for their use. Whatever the ecological and economic arguments might be about how best to manage predator–fisheries interactions, ecologists and economists cannot ignore the shifting balance of public opinion. However elegant the ecosystem models turn out to be, they are nothing without public support for the underlying assumption, that use outweighs delight. Ian L. Boyd British Antarctic Survey, High Cross, Madingley Road, Cambridge, UK CB3 0ET. e-mail: [email protected] References 1 Yodzis, P. (2001) Must top predators be culled for the sake of fisheries? Trends Ecol. Evol. 16, 78–83 2 Homgren, M. et al. (2001) El Niño effects on the dynamics of terrestrial ecosystems. Trends Ecol. Evol. 16, 89–94 3 Sherman, K. (1991) The large marine ecosystem concept: research and management strategy for living marine resources. Ecol. Appl. 1, 349–360 4 Polovina, J.J. et al. (1995) Decadal and basin-scale variation in mixed layer depth and the impact on biological production in the central North Pacific, 1960–88. Deep-Sea Res. 42, 1701–1716 5 White, W.B. and Peterson, R.G. (1996) An Antarctic circumpolar wave in surface pressure, wind, temperature and sea-ice extent. Nature 380, 699–702 6 Rodwell, M.J. et al. (1999) Oceanic forcing of the wintertime North Atlantic oscillation and European climate. Nature 398, 320–323 7 Sakshaug, E. et al. (1994) Structure, biomass distribution, and energetics of the pelagic ecosystem in the Barents Sea: a synopsis. Polar Biol. 14, 405–411 8 Dickson, B. (1997) From the Labrador Sea to global change. Nature 386, 649–650 9 Trillmich, F. and Limberger, D. (1985) Drastic effects of El Niño on Galapagos pinnipeds. Oecologia 67, 19–22
TRENDS in Ecology & Evolution Vol.16 No.6 June 2001
10 Aebischer, N.J. et al. (1990) Parallel long-term trends across four marine trophic levels and weather. Nature 347, 753–755 11 Anon. (1996) The Bering Sea Ecosystem, National Research Council, National Academy Press 12 Trites, A.W. et al. (1999) Ecosystem change and the decline of marine mammals in the Eastern Bering Sea: testing the ecosystem shift and commercial whaling hypothesis. University of British Columbia Fisheries Centre Research Reports 7, 1–106 13 Baumgartner, T.R. et al. (1992) Reconstruction of the history of Pacific sardine and northern anchovy populations over the past two millennia from sediments of the Santa Barbara Basin, California. Cali. Coop. Oceanic Fish. Invest. Rep. 33, 24–40 14 Smout, T.C. (2000) Nature Contested: Environmental History in Scotland and Northern Ireland Since 1600, Edinburgh University Press
Culling predators to protect fisheries: a case of accumulating uncertainties Response from Yodzis
Boyd1 raises an interesting and relevant issue that was barely touched upon in my article, and I thank him for broadening the discussion in this way. There is, indeed, significant physical forcing of some ecosystems, including marine ones. Although physical forcing is a factor that certainly needs to be taken into account, there is, at least in the context of top predator–fishery interactions, little evidence of the dominant role suggested by Boyd. He cites the case of declining Steller sea lions in the Bering Sea and Gulf of Alaska. It is widely accepted that a large-scale environmental change occurred in this system in 1976–1977. However, most scientists concerned with the system, including the authors of one of the sources2 cited by Boyd, feel that the decline has been brought about by a combination of factors, possibly including both environmental change and fishing, not, as stated by Boyd, that ‘large-scale environmental change was as likely to have been the cause [my emphasis] of the declining sea lion population as any interaction with the commercial fishery’. If any documents deserve to be called ‘authoritative’ here, they are the Biological Opinions produced by the National Marine Fisheries Service (NMFS), which is the body explicitly charged with the responsibility to weigh
all the available evidence and to recommend to the US Government a course of action, which will then have the force of law. These reports, particularly the most recent (November 2000: http:// www.fakr.noaa.gov/protectedresources/ stellers/plb/default.htm), although acknowledging that the climate shift might have played some role in the decline of sea lions, reject the hypothesis that it could have been ‘the cause’ of the decline, and, although unable to establish a direct connection between the fishery and the declining population of sea lions, find sufficiently strong indirect evidence that NMFS feels compelled to impose restrictions on the fishery in the hope of reversing the decline. With respect to the viewpoint adopted in my article, the need to understand and cope with environmental change is yet another reason why the admittedly daunting task of multispecies modeling must be attempted. How else to understand ‘what leads to large-scale shifts in the energy flow within these ecosystems’, as Boyd advocates? Conventional wisdom is that the direct effects of climate change are on lower trophic levels, with those effects propagating through the food web to higher trophic levels. As stated in my article (‘it is not difficult to model…environmental variation’), it is perfectly feasible to force multispecies models through parameters that are particularly susceptible to large-scale climate change, just as the actual systems themselves are forced. There has been considerable recent work3–9 on the influence of ‘coloured’ noise (such as oceanic systems appear to experience10,11) on population dynamics, and this research will doubtless be extended to community models. Adding to this theoretical work is the submission for publication of two extensive surveys/analyses (one from my lab) of the empirical literature on long-term time series of environmental variables; experimental work designed to test the theory has also appeared12. Although we have yet to solve these problems, we already have an important insight to add to Horace’s thoughts in the 1st Century BC. Multispecies modeling has shown that use and delight are not necessarily, not always conflicting viewpoints. In the case of the Benguela system discussed in my article, the
http://tree.trends.com 0169–5347/01/$ – see front matter © 2001 Elsevier Science Ltd. All rights reserved.
News & Comment
current most plausible possibility is that those who delight in the presence of fur seals in that system and those who would use hake fishes there need not do so at one another’s expense. Peter Yodzis Dept of Zoology, University of Guelph, Guelph, Ontario, Canada N1G 2W1. e-mail: [email protected] References 1 Boyd, I.L. (2001) Culling predators to protect fisheries: a case of accumulating uncertainties. Trends Ecol. Evol. 16, 281–282 2 Anon. (1996) The Bering Sea Ecosystem, National Research Council, National Academy Press 3 Steele, J.H. and Henderson, E.W. (1984) Modeling long-term fluctuations in fish stocks. Science 224, 985–987 4 Halley, J.M. and Kunin, W.E. (1996) Extinction risk and the 1/f family of noise models. Theor. Popul. Biol. 56, 215–230 5 Ripa, J. and Lundberg, P. (1996) Noise colour and the risk of extinctions. Proc. R. Soc. London B Biol. Sci. 263, 1751–1753 6 Johst, K. and Wissel, C. (1997) Extinction risk in a temporally correlated environment. Theor. Popul. Biol. 52, 91–100 7 Petchey, O.L. et al. (1997) Effects on population persistence: the interaction between environmental noise colour, intraspecific competition and space. Proc. R. Soc. London B Biol. Sci. 264, 1841–1847 8 Cuddington, K. and Yodzis, P. (1999) Black noise and population persistence. Proc. R. Soc. London B Biol. Sci. 266, 969–973 9 Morales, J.M. (1999) Viability in a pink environment: why ‘white noise’ models can be dangerous. Ecol. Lett. 2, 228–232 10 Monin, A.S. et al. (1977) Variability of the Oceans, John Wiley & Sons 11 Steele, J.H. (1985) A comparison of marine and terrestrial ecological systems. Nature 313, 355–358 12 Petchey, O.L. (2000) Environmental colour affects aspects of single-species population dynamics. Proc. R. Soc. London B Biol. Sci. 267, 747–754
Parallel speciation with allopatry In a recent review1, Johannesson argues that parallel speciation is strong evidence for sympatric speciation. Our work on threespine sticklebacks Gasterosteus spp., which provides the clearest example of parallel speciation to date from nature, was cited in support of this view. However, laboratory studies show that parallel speciation can occur between allopatric populations. Furthermore, the weight of evidence indicates an allopatric stage in the origin of the stickleback species.
TRENDS in Ecology & Evolution Vol.16 No.6 June 2001
Parallel speciation is a special case of parallel evolution whereby traits causing reproductive isolation evolve in parallel in independent populations that inhabit similar environments2,3. The process is important because natural selection alone can produce it (the path of genetic drift might sometimes repeat itself in different lineages, but the outcome would not be correlated with environment). Parallel evolution of ordinary phenotypic traits occurs often between allopatric populations, and reproductive isolation could evolve in parallel under the same circumstances, especially if ordinary phenotypic traits underlie reproductive isolation. In support, the two examples of parallel evolution of reproductive isolation in the laboratory involved wholly allopatric populations4,5. Sympatric limnetic and benthic threespine sticklebacks probably have multiple independent origins6,7, and morphological similarities between limnetics and between benthics from different lakes represent parallel evolution. Sympatric forms rarely, if ever, hybridize in the wild, and therefore constitute good biological species7 (they hybridize at a low rate in no-choice mating trials in the laboratory3). Remarkably, the basis of this reproductive isolation has evolved in parallel. Despite their different evolutionary histories, male and female benthic individuals from different lakes mate just as readily with one another as do male and female individuals from the same population. The result is the same for limnetics. Conversely, limnetics and benthics from different lakes mate infrequently, which is similar to the low frequency of mating between limnetics and benthics from the same lake3. These results represent evidence of parallel speciation in sticklebacks, but they should not be interpreted as evidence of their sympatric speciation. Indeed, the evidence indicates that each stickleback species pair is the result of two separate invasions of freshwater by the ancestral marine species, Gasterosteus aculeatus, near the end of the last ice age. In each case, the first invader led to the present-day benthic species, whereas the second invader led to the present-day limnetic species. The evidence is as follows. First, study of
283
25 allozyme loci from two lakes8,9 indicate that the limnetic species is similar to the present-day marine species (Nei’s D ≈0.02), whereas benthics are more distant (Nei’s D ≈0.07). Second, similar to the marine species, limnetics can successfully develop in seawater (28 ppt salt) from fertilized egg to hatchling stages, whereas benthics develop poorly under these conditions10. This is consistent with two invasions spaced apart in time if salinity tolerance decays gradually after colonization of freshwater. Third, microsatellite evidence fails to support the sympatric speciation scenario7. For example, a phylogeny in which sympatric limnetic and benthic species are constrained to be sister species fits data on allele frequencies at six microsatellite loci significantly worse than does the unconstrained maximum-likelihood phylogeny7. In contrast to these indications of double invasions, RFLP analysis of mitochondrial DNA (mtDNA) is more consistent with sympatric speciation: each lake has unique mtDNA haplotypes that occur at high frequency in both resident species6. Although it is conceivable that the mtDNA data reflect the true population histories, we believe that the discrepancy with other data is the result of low levels of mtDNA gene flow between sympatric limnetic and benthic species after the second invasion6,7. Although there is evidence that premating isolation between stickleback species has been strengthened in sympatry11, initial divergence in morphology, ecology and mate preference probably took place during the allopatric phase. It is probable that divergent natural selection in sympatry allowed the new species to persist and to continue to diverge after the second invasion. Parallel speciation is one source of evidence for divergent natural selection in the origin of stickleback species (‘ecological speciation’), but neither favors nor rules out any specific geographical scenario. Dolph Schluter* Janette W. Boughman Howard D. Rundle Zoology Dept andThe Center for Biodiversity Research,The University of British Columbia, Vancouver, BC, Canada V6T 1Z4. *e-mail: [email protected]
http://tree.trends.com 0169–5347/01/$ – see front matter © 2001 Elsevier Science Ltd. All rights reserved.
News & Comment
interactions. Quite apart from the issues of external forcing of ecosystems, the requirements for large volumes of temporally relevant and expensively obtained data might ultimately rule out the multispecies approach as a practical solution. Finally, perhaps the justification for or against culling predators as a form of fisheries management has greater dimensionality than even the complex food web models described by Yodzis. Since before Horace considered the conflicting paradigms of use and delight for his garden in the 1st Century BC (Ref. 14), people have battled with the difficult balance of utilitarianism versus aestheticism. For a variety of reasons, marine predators currently appeal more for aesthetic reasons than for their use. Whatever the ecological and economic arguments might be about how best to manage predator–fisheries interactions, ecologists and economists cannot ignore the shifting balance of public opinion. However elegant the ecosystem models turn out to be, they are nothing without public support for the underlying assumption, that use outweighs delight. Ian L. Boyd British Antarctic Survey, High Cross, Madingley Road, Cambridge, UK CB3 0ET. e-mail: [email protected] References 1 Yodzis, P. (2001) Must top predators be culled for the sake of fisheries? Trends Ecol. Evol. 16, 78–83 2 Homgren, M. et al. (2001) El Niño effects on the dynamics of terrestrial ecosystems. Trends Ecol. Evol. 16, 89–94 3 Sherman, K. (1991) The large marine ecosystem concept: research and management strategy for living marine resources. Ecol. Appl. 1, 349–360 4 Polovina, J.J. et al. (1995) Decadal and basin-scale variation in mixed layer depth and the impact on biological production in the central North Pacific, 1960–88. Deep-Sea Res. 42, 1701–1716 5 White, W.B. and Peterson, R.G. (1996) An Antarctic circumpolar wave in surface pressure, wind, temperature and sea-ice extent. Nature 380, 699–702 6 Rodwell, M.J. et al. (1999) Oceanic forcing of the wintertime North Atlantic oscillation and European climate. Nature 398, 320–323 7 Sakshaug, E. et al. (1994) Structure, biomass distribution, and energetics of the pelagic ecosystem in the Barents Sea: a synopsis. Polar Biol. 14, 405–411 8 Dickson, B. (1997) From the Labrador Sea to global change. Nature 386, 649–650 9 Trillmich, F. and Limberger, D. (1985) Drastic effects of El Niño on Galapagos pinnipeds. Oecologia 67, 19–22
TRENDS in Ecology & Evolution Vol.16 No.6 June 2001
10 Aebischer, N.J. et al. (1990) Parallel long-term trends across four marine trophic levels and weather. Nature 347, 753–755 11 Anon. (1996) The Bering Sea Ecosystem, National Research Council, National Academy Press 12 Trites, A.W. et al. (1999) Ecosystem change and the decline of marine mammals in the Eastern Bering Sea: testing the ecosystem shift and commercial whaling hypothesis. University of British Columbia Fisheries Centre Research Reports 7, 1–106 13 Baumgartner, T.R. et al. (1992) Reconstruction of the history of Pacific sardine and northern anchovy populations over the past two millennia from sediments of the Santa Barbara Basin, California. Cali. Coop. Oceanic Fish. Invest. Rep. 33, 24–40 14 Smout, T.C. (2000) Nature Contested: Environmental History in Scotland and Northern Ireland Since 1600, Edinburgh University Press
Culling predators to protect fisheries: a case of accumulating uncertainties Response from Yodzis
Boyd1 raises an interesting and relevant issue that was barely touched upon in my article, and I thank him for broadening the discussion in this way. There is, indeed, significant physical forcing of some ecosystems, including marine ones. Although physical forcing is a factor that certainly needs to be taken into account, there is, at least in the context of top predator–fishery interactions, little evidence of the dominant role suggested by Boyd. He cites the case of declining Steller sea lions in the Bering Sea and Gulf of Alaska. It is widely accepted that a large-scale environmental change occurred in this system in 1976–1977. However, most scientists concerned with the system, including the authors of one of the sources2 cited by Boyd, feel that the decline has been brought about by a combination of factors, possibly including both environmental change and fishing, not, as stated by Boyd, that ‘large-scale environmental change was as likely to have been the cause [my emphasis] of the declining sea lion population as any interaction with the commercial fishery’. If any documents deserve to be called ‘authoritative’ here, they are the Biological Opinions produced by the National Marine Fisheries Service (NMFS), which is the body explicitly charged with the responsibility to weigh
all the available evidence and to recommend to the US Government a course of action, which will then have the force of law. These reports, particularly the most recent (November 2000: http:// www.fakr.noaa.gov/protectedresources/ stellers/plb/default.htm), although acknowledging that the climate shift might have played some role in the decline of sea lions, reject the hypothesis that it could have been ‘the cause’ of the decline, and, although unable to establish a direct connection between the fishery and the declining population of sea lions, find sufficiently strong indirect evidence that NMFS feels compelled to impose restrictions on the fishery in the hope of reversing the decline. With respect to the viewpoint adopted in my article, the need to understand and cope with environmental change is yet another reason why the admittedly daunting task of multispecies modeling must be attempted. How else to understand ‘what leads to large-scale shifts in the energy flow within these ecosystems’, as Boyd advocates? Conventional wisdom is that the direct effects of climate change are on lower trophic levels, with those effects propagating through the food web to higher trophic levels. As stated in my article (‘it is not difficult to model…environmental variation’), it is perfectly feasible to force multispecies models through parameters that are particularly susceptible to large-scale climate change, just as the actual systems themselves are forced. There has been considerable recent work3–9 on the influence of ‘coloured’ noise (such as oceanic systems appear to experience10,11) on population dynamics, and this research will doubtless be extended to community models. Adding to this theoretical work is the submission for publication of two extensive surveys/analyses (one from my lab) of the empirical literature on long-term time series of environmental variables; experimental work designed to test the theory has also appeared12. Although we have yet to solve these problems, we already have an important insight to add to Horace’s thoughts in the 1st Century BC. Multispecies modeling has shown that use and delight are not necessarily, not always conflicting viewpoints. In the case of the Benguela system discussed in my article, the
http://tree.trends.com 0169–5347/01/$ – see front matter © 2001 Elsevier Science Ltd. All rights reserved.
News & Comment
current most plausible possibility is that those who delight in the presence of fur seals in that system and those who would use hake fishes there need not do so at one another’s expense. Peter Yodzis Dept of Zoology, University of Guelph, Guelph, Ontario, Canada N1G 2W1. e-mail: [email protected] References 1 Boyd, I.L. (2001) Culling predators to protect fisheries: a case of accumulating uncertainties. Trends Ecol. Evol. 16, 281–282 2 Anon. (1996) The Bering Sea Ecosystem, National Research Council, National Academy Press 3 Steele, J.H. and Henderson, E.W. (1984) Modeling long-term fluctuations in fish stocks. Science 224, 985–987 4 Halley, J.M. and Kunin, W.E. (1996) Extinction risk and the 1/f family of noise models. Theor. Popul. Biol. 56, 215–230 5 Ripa, J. and Lundberg, P. (1996) Noise colour and the risk of extinctions. Proc. R. Soc. London B Biol. Sci. 263, 1751–1753 6 Johst, K. and Wissel, C. (1997) Extinction risk in a temporally correlated environment. Theor. Popul. Biol. 52, 91–100 7 Petchey, O.L. et al. (1997) Effects on population persistence: the interaction between environmental noise colour, intraspecific competition and space. Proc. R. Soc. London B Biol. Sci. 264, 1841–1847 8 Cuddington, K. and Yodzis, P. (1999) Black noise and population persistence. Proc. R. Soc. London B Biol. Sci. 266, 969–973 9 Morales, J.M. (1999) Viability in a pink environment: why ‘white noise’ models can be dangerous. Ecol. Lett. 2, 228–232 10 Monin, A.S. et al. (1977) Variability of the Oceans, John Wiley & Sons 11 Steele, J.H. (1985) A comparison of marine and terrestrial ecological systems. Nature 313, 355–358 12 Petchey, O.L. (2000) Environmental colour affects aspects of single-species population dynamics. Proc. R. Soc. London B Biol. Sci. 267, 747–754
Parallel speciation with allopatry In a recent review1, Johannesson argues that parallel speciation is strong evidence for sympatric speciation. Our work on threespine sticklebacks Gasterosteus spp., which provides the clearest example of parallel speciation to date from nature, was cited in support of this view. However, laboratory studies show that parallel speciation can occur between allopatric populations. Furthermore, the weight of evidence indicates an allopatric stage in the origin of the stickleback species.
TRENDS in Ecology & Evolution Vol.16 No.6 June 2001
Parallel speciation is a special case of parallel evolution whereby traits causing reproductive isolation evolve in parallel in independent populations that inhabit similar environments2,3. The process is important because natural selection alone can produce it (the path of genetic drift might sometimes repeat itself in different lineages, but the outcome would not be correlated with environment). Parallel evolution of ordinary phenotypic traits occurs often between allopatric populations, and reproductive isolation could evolve in parallel under the same circumstances, especially if ordinary phenotypic traits underlie reproductive isolation. In support, the two examples of parallel evolution of reproductive isolation in the laboratory involved wholly allopatric populations4,5. Sympatric limnetic and benthic threespine sticklebacks probably have multiple independent origins6,7, and morphological similarities between limnetics and between benthics from different lakes represent parallel evolution. Sympatric forms rarely, if ever, hybridize in the wild, and therefore constitute good biological species7 (they hybridize at a low rate in no-choice mating trials in the laboratory3). Remarkably, the basis of this reproductive isolation has evolved in parallel. Despite their different evolutionary histories, male and female benthic individuals from different lakes mate just as readily with one another as do male and female individuals from the same population. The result is the same for limnetics. Conversely, limnetics and benthics from different lakes mate infrequently, which is similar to the low frequency of mating between limnetics and benthics from the same lake3. These results represent evidence of parallel speciation in sticklebacks, but they should not be interpreted as evidence of their sympatric speciation. Indeed, the evidence indicates that each stickleback species pair is the result of two separate invasions of freshwater by the ancestral marine species, Gasterosteus aculeatus, near the end of the last ice age. In each case, the first invader led to the present-day benthic species, whereas the second invader led to the present-day limnetic species. The evidence is as follows. First, study of
283
25 allozyme loci from two lakes8,9 indicate that the limnetic species is similar to the present-day marine species (Nei’s D ≈0.02), whereas benthics are more distant (Nei’s D ≈0.07). Second, similar to the marine species, limnetics can successfully develop in seawater (28 ppt salt) from fertilized egg to hatchling stages, whereas benthics develop poorly under these conditions10. This is consistent with two invasions spaced apart in time if salinity tolerance decays gradually after colonization of freshwater. Third, microsatellite evidence fails to support the sympatric speciation scenario7. For example, a phylogeny in which sympatric limnetic and benthic species are constrained to be sister species fits data on allele frequencies at six microsatellite loci significantly worse than does the unconstrained maximum-likelihood phylogeny7. In contrast to these indications of double invasions, RFLP analysis of mitochondrial DNA (mtDNA) is more consistent with sympatric speciation: each lake has unique mtDNA haplotypes that occur at high frequency in both resident species6. Although it is conceivable that the mtDNA data reflect the true population histories, we believe that the discrepancy with other data is the result of low levels of mtDNA gene flow between sympatric limnetic and benthic species after the second invasion6,7. Although there is evidence that premating isolation between stickleback species has been strengthened in sympatry11, initial divergence in morphology, ecology and mate preference probably took place during the allopatric phase. It is probable that divergent natural selection in sympatry allowed the new species to persist and to continue to diverge after the second invasion. Parallel speciation is one source of evidence for divergent natural selection in the origin of stickleback species (‘ecological speciation’), but neither favors nor rules out any specific geographical scenario. Dolph Schluter* Janette W. Boughman Howard D. Rundle Zoology Dept andThe Center for Biodiversity Research,The University of British Columbia, Vancouver, BC, Canada V6T 1Z4. *e-mail: [email protected]
http://tree.trends.com 0169–5347/01/$ – see front matter © 2001 Elsevier Science Ltd. All rights reserved.