- Email: [email protected]
Invasion of fresh waters by saltwater animals
CORRESPONDENCE Still having trouble with relatives Komdeur and Hatchwell’s1 article on kin recognition in avian societies raises important issues about function and mechanism in kin-biased behaviour. Their adaptive life history perspective is, without doubt, a welcome contribution to the kinship debate. However, their arguments might have been more forceful still if they had not continued to promulgate some long-questioned, but remarkably resistant, canons of the kinship literature: namely that kin-biased altruism implies kin discrimination based on kin recognition, and that kin recognition mechanisms can be divided into the four categories of recognition alleles, phenotype matching, associative learning (familiarity) and spatially based recognition2. It is nearly ten years since the publication of Grafen’s3 incisive paper ‘Do animals really recognize kin?’ and subsequent papers related to it4,5, and a little more than that since the first critiques of the classical mechanisms of kin recognition6–10. Although some of these papers, especially Grafen’s3, are cited widely, their messages are rarely taken home. Grafen’s3 central point is simple: although there are undoubtedly many examples of kin bias (e.g. cooperative breeding in certain bird species), only those involving recognition of relatedness per se (i.e. genetic similarity), with the purpose of biasing responses towards relatives (kin discrimination), deserve the label ‘kin recognition’3,5,8,10. Other examples, although correlating with genetic similarity or even being based on recognition of similarity, might actually be for purposes other than discriminating relatives. Any such kinship effect is incidental and does not constitute kin discrimination, let alone a special mechanism of kin recognition. This is not a semantic issue or a terminological whim. It makes a crucial difference to the interpretation of kin bias outside the boundaries of inclusive fitness theory, optimal inbreeding and/or optimal outbreeding and reciprocity; it is also eminently testable11,12. Of course, Komdeur and Hatchwell might be right and there might not be any incidental kin bias in cooperatively breeding birds, but the social structure and development of these species certainly raise the possibility. Naturally, if kinship effects turn out to be incidental, any posited mechanisms of kin discrimination become redundant. However, even if kin discrimination (whether based on kin recognition or recognition of some other category correlating kinship9) is demonstrated, the four categories of recognition mechanisms are not helpful for two reasons: first they do not constitute a set of mutually exclusive alternatives6,7, and second they confuse questions about the development and expression of traits indicating genetic similarity with those about the processes of perceiving and acting upon this information6,7,9. Classifications have been proposed that avoid these pitfalls8,9, which would prevent the perpetuation of historical confusions regarding kinship issues.
448
Chris Barnard Behaviour and Ecology Research Group, School of Biological Sciences, University of Nottingham, University Park, Nottingham, UK NG7 2RD ([email protected]) References 1 Komdeur, J. and Hatchwell, B.J. (1999) Trends Ecol. Evol. 14, 237–241 2 Holmes, W.G. and Sherman, P.W. (1983) Am. Sci. 71, 46–55 3 Grafen, A. (1990) Anim. Behav. 39, 42–54 4 Grafen, A. (1991) Anim. Behav. 41, 1095–1096 5 Barnard, C.J., Hurst, J.L. and Aldhous, P.G.M. (1991) Biol. Rev. 66, 379–430 6 Fletcher, D.J.C. (1987) in Kin Recognition in Animals (Fletcher, D.J.C. and Michener, C.D., eds), pp. 19–54, Wiley 7 Waldman, B. (1987) J. Theor. Biol. 128, 159–185 8 Waldman, B., Frumhoff, P.C. and Sherman, P.W. (1988) Trends Ecol. Evol. 3, 8–13 9 Barnard, C.J. (1990) Adv. Stud. Behav. 19, 29–81 10 Barnard, C.J. (1991) Trends Ecol. Evol. 6, 310–311 11 Pfennig, D. (1990) Evolution 44, 785–798 12 Hurst, J.L. and Barnard, C.J. (1995) Behav. Ecol. Sociobiol. 36, 333–342
incidental (see Box 1; Ref. 2). The four categories of recognition mechanisms that we considered in our article are helpful in trying to understand these examples of kin preference, whether or not kin discrimination is demonstrated. Although we realize that kin recognition through phenotype matching might involve recognition alleles, we feel that kin discrimination either through phenotype matching and/or recognition alleles, associative learning and spatially based recognition are heuristically useful and, importantly, from an empirical perspective, they make exclusive predictions about where helpers should direct their care. We sought to emphasize that the nature and precision of cues for discrimination available to helpers will vary with the ecology and life history of particular species, and are unlikely to be universal.
Jan Komdeur Dept of Animal Ecology, University of Groningen, PO Box 14, 9750 AA Haren, The Netherlands ([email protected])
Ben J. Hatchwell Dept of Animal and Plant Sciences, University of Sheffield, Sheffield, UK S10 2TN ([email protected]) References
Reply from J. Komdeur and B.J. Hatchwell We welcome Barnard’s comments1 regarding our article2 on kin recognition in avian societies. Indeed, we agree that certain arguments about the function and mechanism of kin-biased behaviour would be more forceful without referring to the long-questioned but nevertheless, resistant tenets of the kinship literature. However, we feel that this is necessary for a proper evaluation of the experimental evidence for kin discrimination, and to discuss the mechanism and adaptive value of kin recognition in cooperative and noncooperative species. For a nonbreeding helper to maximize fitness by providing aid to their closest genetic relatives, it is crucial to discriminate between kin and non-kin, and even between kin differing in their degree of relatedness. If using a strict definition of ‘kin recognition’ (kin discrimination through recognition of relatedness), we agree with Barnard that ‘kinrecognition’ is not the sole mechanism to achieve kin discrimination. In our review, we have defined the term kin recognition as the ability to discriminate between kin and non-kin either through strict ‘kin recognition’ or through other mechanisms (e.g. associative learning). Whatever definition or terminology is used, the messages of our review remain the same: that associative learning is the most likely mechanism enabling helpers to discriminate kin from non-kin; and, that there is a lack of empirical studies in this area. Helpers of several cooperatively breeding bird species preferentially allocate their aid to closest kin3, suggesting that kinship effects are not
0169-5347/99/$ – see front matter © 1999 Elsevier Science Ltd. All rights reserved.
1 Barnard, C. (1999) Trends Ecol. Evol. 14, 448 2 Komdeur, J. and Hatchwell, B.J. (1999) Trends Ecol. Evol. 14, 237–241 3 Emlen, S.T. (1997) in Behavioural Ecology: An Evolutionary Approach (Krebs, J.R. and Davies, N.B., eds), pp. 228–253, Cambridge University Press
Invasion of fresh waters by saltwater animals In Lee and Bell’s recent TREE perspective1 on recent invasions of fresh waters by saltwater animals, they mis-stated the invasion history of the zebra mussel (Dreissena polymorpha) and overstated the role of humans in causing marine and brackish-water animals to invade fresh waters. Lee and Bell listed the zebra mussel as a marine or brackish-water species that invaded fresh waters after 1800 as a result of shipping traffic. In fact, the natural range of zebra mussels (i.e. before 1800) included many fresh waters in southeastern Europe, such as Lakes Ohrid and Prespa and the lower courses of various rivers (e.g. the Volga, Danube and Ural2,3), as well as brackish waters such as the Caspian Sea [,6–9 parts per thousand (ppt) salinity], Aral Sea (10–12 ppt) and estuaries of the Black Sea (0–2 ppt)4. In addition, during preglacial and interglacial times, zebra mussels were distributed widely in fresh waters throughout Europe and Asia Minor2,5. At no time have zebra mussels, or any other member of the genus Dreissena, been found in marine waters2,6. TREE vol. 14, no. 11 November 1999
CORRESPONDENCE In the early 19th century, humans built canals to link the rivers of the Caspian Sea basin with tributaries of the Baltic Sea, and shipping traffic through this, and other, canals allowed zebra mussels to spread rapidly through central and western Europe2. Shipping activities subsequently brought zebra mussels to North America, where they now flourish. Thus, human activities allowed zebra mussels to move between freshwater drainage basins, but not to make the initial transition from saltwater to freshwater. Several other species, listed by Lee and Bell as examples of recent, human-caused invasions of fresh waters, probably also invaded fresh waters well before 1800 without human help. For instance, Cordylophora caspia, C. lacustris (probably a synonym of C. caspia), Corophium curvispinum and Echinogammarus ischnus were said by Lee and Bell to have entered freshwater between 1854 and 1931. However, by the early 1900s, these three species were reported to be common and widespread in lakes and rivers throughout the Black and Caspian Sea basins, from Turkey to the Urals7–9. It seems unlikely that this distribution could have been achieved if these species had entered freshwater only in the past 200 years as a result of recent human activities. Instead, these species probably have lived in freshwater ‘since ancient times’7. Undoubtedly, human activities have led to some important invasions of fresh waters by saltwater animals, but Lee and Bell overestimate the frequency of such human-caused invasions. This overestimate undermines parts of Lee and Bell’s conclusions, including their assertion that ‘many highly invasive and disruptive species in freshwater are recent immigrants from saline habitats’. Several of the most disruptive invaders (e.g. D. polymorpha, C. curvispinum, E. ischnus) entered fresh waters in prehistoric times without human intervention. Human activities have moved many freshwater pest species into new ranges, but this movement has been largely from one freshwater basin to another, not from salt waters to fresh waters.
David Strayer Institute of Ecosystem Studies, PO Box AB, Millbrook, NY 12545, USA ([email protected]) References 1 Lee, C.E. and Bell, M.A. (1999) Trends Ecol. Evol. 14, 284–288 2 Kinzelbach, R. (1992) in The Zebra Mussel Dreissena polymorpha (Neumann, D. and Jenner, H.A., eds), pp. 5–17, Gustav Fischer Verlag 3 Ehrmann, P. (1933) in Die Tierwelt Mitteleuropas. Mollusken (Weichtiere) (Brohmer, P. et al., eds), Verlag Von Quelle & Meyer 4 Strayer, D.L. and Smith, L.C. (1993) in Zebra Mussels: Biology, Impacts, and Control (Nalepa, T.F. and Schloesser, D.W., eds), pp. 715–727, Lewis Publishers 5 Kinzelbach, R. (1986) Zool. Middle East 1, 132–138 6 Bânârescu, P. (1990) Zoogeography of Fresh Waters (Vol. 1), AULA-Verlag 7 Mordukhai-Boltovskoi, P.D. (1964) Int. Rev. Ges. Hydrobiol. 49, 139–176 8 Mordukhai-Boltovskoi, P.D. (1979) Int. Rev. Ges. Hydrobiol. 64, 1–38 9 Hutchinson, G.E. (1967) A Treatise on Limnology, (Vol. 2), Wiley TREE vol. 14, no. 11 November 1999
Reply from C.E. Lee and M.A. Bell Strayer states that we erred in the dates we gave for the initial colonizations of fresh water1. However, our goal was not to document initial dates of freshwater invasions, but rather to discuss cases where there is evidence for recent habitat shifts by particular populations, independent of prior invasions by other populations. What we emphasize in our paper are the remarkable facts that (1) colonizations from salt water (brackish or marine) can occur on decadal rather than on millennial time scales, and (2) that recent immigrants from salt water can spread rapidly and persist in fresh water, through facilitation by humans. Table 1 of our perspective article1 lists examples for which timing and direction of invasions can be inferred from concrete evidence (the criteria for the examples we use are given in Box 1), rather than examples of first appearances in fresh water. For instance, for the copepod Eurytemora affinis, we list several dates, from the 1930s to the 1980s. These are not dates this species first entered fresh water but inferred dates of repeated and independent invasions from saltwater sources2. Strayer highlights the problem of using species distributions to infer pathways of freshwater invasions, especially when systematic relationships among populations are uncertain. For instance, in the case of the zebra mussel Dreissena polymorpha, the extent to which postglacial freshwater populations survived to the present day is inconclusive3. In addition, populations from southwestern Europe, such as those in Lakes Ohrid and Prespa, are thought to represent ancient invasions of fresh water, and are considered sibling species of populations from the Ponto-Caspian basin3,4, the likely source of recent invasions5,6. As stated in our paper, genetic markers would be required to determine pathways and frequency of invasions, and in the case of D. polymorpha, clarify systematic relationships among populations and sibling species. The impact of humans in the past 200 years should not be underestimated. The direct transfer of organisms (including those that Strayer mentions) from salt water to fresh water has occurred on massive scales, and many of these cases are documented1. For example, in Eastern Europe and Russia large-scale acclimatization of numerous Ponto-Caspian species into freshwater reservoirs was undertaken for aquaculture purposes7,8. In addition, impoundment of entire
bays and lagoons resulted in the large-scale trapping and acclimatization of populations9,10. Physiological studies indicate that these invaders are energetically less efficient in fresh water than more ancient freshwater species11,12. Yet, the creation of reservoirs (as havens for acclimation and as stepping stones) and transport vectors has extended their ranges7,8 and made invasions from saline habitats more likely and serious. The implication is that within the modern era we can expect many more independent invasions to occur from saline to freshwater habitats, especially from the Ponto-Caspian region. Human transport and habitat alteration have accelerated the pace of such invasions, and they have the potential for major impacts on aquatic ecosystems.
Carol Eunmi Lee Marine Biology Research Division 0202, Scripps Institution of Oceanography, University of California, San Diego, La Jolla, CA 92093-0202, USA ([email protected])
Michael A. Bell Dept of Ecology and Evolution, State University of New York, Stony Brook, NY 11794-5245, USA ([email protected]) References 1 Lee, C.E. and Bell, M.A. (1999) Trends Ecol. Evol. 14, 284–288 2 Lee, C.E. Evolution (in press) 3 Kinzelbach, R. (1992) in The Zebra Mussel Dreissena polymorpha (Neumann, D. and Jenner, H.A., eds), pp. 5–17, Gustav Fischer Verlag 4 Kinzelbach, R. (1986) Zool. Middle East 1, 132–138 5 De Martonne, E. (1927) Trait de Geographie Physique, Librairie Armand Colin 6 Rosenberg, G. and Ludyanskiy, M.L. (1994) Can. J. Fish. Aquat. Sci. 51, 1474–1484 7 Mordukhai-Boltovskoi, P.D. (1979) Int. Rev. Gesamten Hydrobiol. 64, 1–38 8 Jazdzewski, K. (1980) Crustaceana (Suppl.) 6, 84–107 9 De Beaufort, L.F. (1954) Veranderingen in de Flora en Fauna van de Zuiderzee (thans IJsselmeer) na de Afsluiting in 1932, C. de Boer, Jr 10 Miller, R.C. (1958) J. Mar. Res. 17, 375–382 11 Taylor, P.M. and Harris, R.R. (1986) J. Comp. Physiol. 156, 323–329 12 McMahon, R.F. (1996) Am. Zool. 36, 339–363
Corrigendum Luikart, G. and England, P.R. Trends Ecol. Evol. 14, 253–256 (July 1999) In Table 1, the correct source of the CERVUS program for assigning paternity and inferring parentage should be:
http://helios.bto.ed.ac.uk/evolgen
0169-5347/99/$ – see front matter © 1999 Elsevier Science Ltd. All rights reserved.
PII: S0169-5347(99)01739-5
449
448
Chris Barnard Behaviour and Ecology Research Group, School of Biological Sciences, University of Nottingham, University Park, Nottingham, UK NG7 2RD ([email protected]) References 1 Komdeur, J. and Hatchwell, B.J. (1999) Trends Ecol. Evol. 14, 237–241 2 Holmes, W.G. and Sherman, P.W. (1983) Am. Sci. 71, 46–55 3 Grafen, A. (1990) Anim. Behav. 39, 42–54 4 Grafen, A. (1991) Anim. Behav. 41, 1095–1096 5 Barnard, C.J., Hurst, J.L. and Aldhous, P.G.M. (1991) Biol. Rev. 66, 379–430 6 Fletcher, D.J.C. (1987) in Kin Recognition in Animals (Fletcher, D.J.C. and Michener, C.D., eds), pp. 19–54, Wiley 7 Waldman, B. (1987) J. Theor. Biol. 128, 159–185 8 Waldman, B., Frumhoff, P.C. and Sherman, P.W. (1988) Trends Ecol. Evol. 3, 8–13 9 Barnard, C.J. (1990) Adv. Stud. Behav. 19, 29–81 10 Barnard, C.J. (1991) Trends Ecol. Evol. 6, 310–311 11 Pfennig, D. (1990) Evolution 44, 785–798 12 Hurst, J.L. and Barnard, C.J. (1995) Behav. Ecol. Sociobiol. 36, 333–342
incidental (see Box 1; Ref. 2). The four categories of recognition mechanisms that we considered in our article are helpful in trying to understand these examples of kin preference, whether or not kin discrimination is demonstrated. Although we realize that kin recognition through phenotype matching might involve recognition alleles, we feel that kin discrimination either through phenotype matching and/or recognition alleles, associative learning and spatially based recognition are heuristically useful and, importantly, from an empirical perspective, they make exclusive predictions about where helpers should direct their care. We sought to emphasize that the nature and precision of cues for discrimination available to helpers will vary with the ecology and life history of particular species, and are unlikely to be universal.
Jan Komdeur Dept of Animal Ecology, University of Groningen, PO Box 14, 9750 AA Haren, The Netherlands ([email protected])
Ben J. Hatchwell Dept of Animal and Plant Sciences, University of Sheffield, Sheffield, UK S10 2TN ([email protected]) References
Reply from J. Komdeur and B.J. Hatchwell We welcome Barnard’s comments1 regarding our article2 on kin recognition in avian societies. Indeed, we agree that certain arguments about the function and mechanism of kin-biased behaviour would be more forceful without referring to the long-questioned but nevertheless, resistant tenets of the kinship literature. However, we feel that this is necessary for a proper evaluation of the experimental evidence for kin discrimination, and to discuss the mechanism and adaptive value of kin recognition in cooperative and noncooperative species. For a nonbreeding helper to maximize fitness by providing aid to their closest genetic relatives, it is crucial to discriminate between kin and non-kin, and even between kin differing in their degree of relatedness. If using a strict definition of ‘kin recognition’ (kin discrimination through recognition of relatedness), we agree with Barnard that ‘kinrecognition’ is not the sole mechanism to achieve kin discrimination. In our review, we have defined the term kin recognition as the ability to discriminate between kin and non-kin either through strict ‘kin recognition’ or through other mechanisms (e.g. associative learning). Whatever definition or terminology is used, the messages of our review remain the same: that associative learning is the most likely mechanism enabling helpers to discriminate kin from non-kin; and, that there is a lack of empirical studies in this area. Helpers of several cooperatively breeding bird species preferentially allocate their aid to closest kin3, suggesting that kinship effects are not
0169-5347/99/$ – see front matter © 1999 Elsevier Science Ltd. All rights reserved.
1 Barnard, C. (1999) Trends Ecol. Evol. 14, 448 2 Komdeur, J. and Hatchwell, B.J. (1999) Trends Ecol. Evol. 14, 237–241 3 Emlen, S.T. (1997) in Behavioural Ecology: An Evolutionary Approach (Krebs, J.R. and Davies, N.B., eds), pp. 228–253, Cambridge University Press
Invasion of fresh waters by saltwater animals In Lee and Bell’s recent TREE perspective1 on recent invasions of fresh waters by saltwater animals, they mis-stated the invasion history of the zebra mussel (Dreissena polymorpha) and overstated the role of humans in causing marine and brackish-water animals to invade fresh waters. Lee and Bell listed the zebra mussel as a marine or brackish-water species that invaded fresh waters after 1800 as a result of shipping traffic. In fact, the natural range of zebra mussels (i.e. before 1800) included many fresh waters in southeastern Europe, such as Lakes Ohrid and Prespa and the lower courses of various rivers (e.g. the Volga, Danube and Ural2,3), as well as brackish waters such as the Caspian Sea [,6–9 parts per thousand (ppt) salinity], Aral Sea (10–12 ppt) and estuaries of the Black Sea (0–2 ppt)4. In addition, during preglacial and interglacial times, zebra mussels were distributed widely in fresh waters throughout Europe and Asia Minor2,5. At no time have zebra mussels, or any other member of the genus Dreissena, been found in marine waters2,6. TREE vol. 14, no. 11 November 1999
CORRESPONDENCE In the early 19th century, humans built canals to link the rivers of the Caspian Sea basin with tributaries of the Baltic Sea, and shipping traffic through this, and other, canals allowed zebra mussels to spread rapidly through central and western Europe2. Shipping activities subsequently brought zebra mussels to North America, where they now flourish. Thus, human activities allowed zebra mussels to move between freshwater drainage basins, but not to make the initial transition from saltwater to freshwater. Several other species, listed by Lee and Bell as examples of recent, human-caused invasions of fresh waters, probably also invaded fresh waters well before 1800 without human help. For instance, Cordylophora caspia, C. lacustris (probably a synonym of C. caspia), Corophium curvispinum and Echinogammarus ischnus were said by Lee and Bell to have entered freshwater between 1854 and 1931. However, by the early 1900s, these three species were reported to be common and widespread in lakes and rivers throughout the Black and Caspian Sea basins, from Turkey to the Urals7–9. It seems unlikely that this distribution could have been achieved if these species had entered freshwater only in the past 200 years as a result of recent human activities. Instead, these species probably have lived in freshwater ‘since ancient times’7. Undoubtedly, human activities have led to some important invasions of fresh waters by saltwater animals, but Lee and Bell overestimate the frequency of such human-caused invasions. This overestimate undermines parts of Lee and Bell’s conclusions, including their assertion that ‘many highly invasive and disruptive species in freshwater are recent immigrants from saline habitats’. Several of the most disruptive invaders (e.g. D. polymorpha, C. curvispinum, E. ischnus) entered fresh waters in prehistoric times without human intervention. Human activities have moved many freshwater pest species into new ranges, but this movement has been largely from one freshwater basin to another, not from salt waters to fresh waters.
David Strayer Institute of Ecosystem Studies, PO Box AB, Millbrook, NY 12545, USA ([email protected]) References 1 Lee, C.E. and Bell, M.A. (1999) Trends Ecol. Evol. 14, 284–288 2 Kinzelbach, R. (1992) in The Zebra Mussel Dreissena polymorpha (Neumann, D. and Jenner, H.A., eds), pp. 5–17, Gustav Fischer Verlag 3 Ehrmann, P. (1933) in Die Tierwelt Mitteleuropas. Mollusken (Weichtiere) (Brohmer, P. et al., eds), Verlag Von Quelle & Meyer 4 Strayer, D.L. and Smith, L.C. (1993) in Zebra Mussels: Biology, Impacts, and Control (Nalepa, T.F. and Schloesser, D.W., eds), pp. 715–727, Lewis Publishers 5 Kinzelbach, R. (1986) Zool. Middle East 1, 132–138 6 Bânârescu, P. (1990) Zoogeography of Fresh Waters (Vol. 1), AULA-Verlag 7 Mordukhai-Boltovskoi, P.D. (1964) Int. Rev. Ges. Hydrobiol. 49, 139–176 8 Mordukhai-Boltovskoi, P.D. (1979) Int. Rev. Ges. Hydrobiol. 64, 1–38 9 Hutchinson, G.E. (1967) A Treatise on Limnology, (Vol. 2), Wiley TREE vol. 14, no. 11 November 1999
Reply from C.E. Lee and M.A. Bell Strayer states that we erred in the dates we gave for the initial colonizations of fresh water1. However, our goal was not to document initial dates of freshwater invasions, but rather to discuss cases where there is evidence for recent habitat shifts by particular populations, independent of prior invasions by other populations. What we emphasize in our paper are the remarkable facts that (1) colonizations from salt water (brackish or marine) can occur on decadal rather than on millennial time scales, and (2) that recent immigrants from salt water can spread rapidly and persist in fresh water, through facilitation by humans. Table 1 of our perspective article1 lists examples for which timing and direction of invasions can be inferred from concrete evidence (the criteria for the examples we use are given in Box 1), rather than examples of first appearances in fresh water. For instance, for the copepod Eurytemora affinis, we list several dates, from the 1930s to the 1980s. These are not dates this species first entered fresh water but inferred dates of repeated and independent invasions from saltwater sources2. Strayer highlights the problem of using species distributions to infer pathways of freshwater invasions, especially when systematic relationships among populations are uncertain. For instance, in the case of the zebra mussel Dreissena polymorpha, the extent to which postglacial freshwater populations survived to the present day is inconclusive3. In addition, populations from southwestern Europe, such as those in Lakes Ohrid and Prespa, are thought to represent ancient invasions of fresh water, and are considered sibling species of populations from the Ponto-Caspian basin3,4, the likely source of recent invasions5,6. As stated in our paper, genetic markers would be required to determine pathways and frequency of invasions, and in the case of D. polymorpha, clarify systematic relationships among populations and sibling species. The impact of humans in the past 200 years should not be underestimated. The direct transfer of organisms (including those that Strayer mentions) from salt water to fresh water has occurred on massive scales, and many of these cases are documented1. For example, in Eastern Europe and Russia large-scale acclimatization of numerous Ponto-Caspian species into freshwater reservoirs was undertaken for aquaculture purposes7,8. In addition, impoundment of entire
bays and lagoons resulted in the large-scale trapping and acclimatization of populations9,10. Physiological studies indicate that these invaders are energetically less efficient in fresh water than more ancient freshwater species11,12. Yet, the creation of reservoirs (as havens for acclimation and as stepping stones) and transport vectors has extended their ranges7,8 and made invasions from saline habitats more likely and serious. The implication is that within the modern era we can expect many more independent invasions to occur from saline to freshwater habitats, especially from the Ponto-Caspian region. Human transport and habitat alteration have accelerated the pace of such invasions, and they have the potential for major impacts on aquatic ecosystems.
Carol Eunmi Lee Marine Biology Research Division 0202, Scripps Institution of Oceanography, University of California, San Diego, La Jolla, CA 92093-0202, USA ([email protected])
Michael A. Bell Dept of Ecology and Evolution, State University of New York, Stony Brook, NY 11794-5245, USA ([email protected]) References 1 Lee, C.E. and Bell, M.A. (1999) Trends Ecol. Evol. 14, 284–288 2 Lee, C.E. Evolution (in press) 3 Kinzelbach, R. (1992) in The Zebra Mussel Dreissena polymorpha (Neumann, D. and Jenner, H.A., eds), pp. 5–17, Gustav Fischer Verlag 4 Kinzelbach, R. (1986) Zool. Middle East 1, 132–138 5 De Martonne, E. (1927) Trait de Geographie Physique, Librairie Armand Colin 6 Rosenberg, G. and Ludyanskiy, M.L. (1994) Can. J. Fish. Aquat. Sci. 51, 1474–1484 7 Mordukhai-Boltovskoi, P.D. (1979) Int. Rev. Gesamten Hydrobiol. 64, 1–38 8 Jazdzewski, K. (1980) Crustaceana (Suppl.) 6, 84–107 9 De Beaufort, L.F. (1954) Veranderingen in de Flora en Fauna van de Zuiderzee (thans IJsselmeer) na de Afsluiting in 1932, C. de Boer, Jr 10 Miller, R.C. (1958) J. Mar. Res. 17, 375–382 11 Taylor, P.M. and Harris, R.R. (1986) J. Comp. Physiol. 156, 323–329 12 McMahon, R.F. (1996) Am. Zool. 36, 339–363
Corrigendum Luikart, G. and England, P.R. Trends Ecol. Evol. 14, 253–256 (July 1999) In Table 1, the correct source of the CERVUS program for assigning paternity and inferring parentage should be:
http://helios.bto.ed.ac.uk/evolgen
0169-5347/99/$ – see front matter © 1999 Elsevier Science Ltd. All rights reserved.
PII: S0169-5347(99)01739-5
449