- Email: [email protected]
Implications of ‘supply-side’ ecology for environmental assessment and management
TREE vol. 6, no. 2, February
even internally - fortunately, one might say. Differences on the level of specific issues stimulate theoretical analyses, comparative empirical studies and experiments, and thus serve as fuel for scientific progress. Acknowledgements Sincerest thanks to Stephen Cousins, Lennart Persson, Stuart P i m m and Robert Vadas for constructive critiques, clarifications of their viewpoints and for suggestions of useful references.
References 1 Patten, B.C. and Odum, E.P. (1981) Am. Nat. 118.886-895 2 Odum; E.P. and Biever, L.J. (1984) Am. Nat. 124,360-376 3 Cousins. S. (1987) Trends Ecol. Evol. 2. 312-316 4 Vadas, R.L., Jr (1989) Oikos 56, 339-343 5 Oksanen, L. (1988) Am. Nat. 131, 424-444 6 Odum, E.P. (1971) Fundamentals of Ecology (3rd edn), W.B. Saunders 7 Odum. H.T. 11960) Am. SC;. 48, l-8 8 Odum, H.T. (1971) Environment, Power and Society, Wiley & Sons 9 Ulanowicz, R.E. (1990) Oikos 57,42-48 IO Hairston, N.G., Smith, F.E. and
Slobodkin, L.B. (1960) Am. Nat. 94, 421-425 11 Slobodkin, L.B., Smith, F.E. and Hairston, N.C. (1967) Am. Nat 101, 109-124 12 Fretwell, S.D. (1977) Perspect. Biol. Med. 20, ‘I69-l 85 13 Oksanen, L., Fretwell, SD., Arruda, J. and Niemela, P. (1981) Am. Nat. 118, 240-261 14 Fretwell, S.D. (1987) Oikos 50, 291-301 15 Oksanen, L. and Ericson, L. (1987) Oikos 50,417-422 16 Oksanen, L. (1990) Oikos 57, 14-24 17 Oksanen, T. (1990) Evol. Ecol. 4, 220-234 18 Persson, L., Andersson, G., Hamrin, S.F. and Johansson, L. (1988) in Complex interactions in Lake Communities (Carpenter, S.R., ed.), pp. 45-65, Springer-Verlag 19 Carpenter, S.R., Kitchell, J.F. and Hogson, J.R. (1985) Bioscience 35, 634-639 20 Murdoch, W.W. (1966) Am. Nat. 100, 219-226 21 Ehrlich, P.R. and Birch, L.C. (1967) Am. Nat. 101,97-107 22 Schoener, T.W. (1983) Am. Nat. 122, 240-285 23 Schoener, T.W. (1985) Am. Nat. 125, 730-740 24 Walter, H. (1968) Die Vegetation der
implications of ‘Supply-side’ Ecologyfor Envirorkhtal Assessment andManagement PeterG, Fairweather Recent work iti marine ecology has reaffirmed UM insight from fisheries science that knowledge about the production, dissemination and success of propagules can guide our management of populations and assemblages. Understanding the variable nature
of recruitment
rebtionships
can
both aid and hinder attempts at environmental monitoring, rehabilitation and innovative selection of marine reserves. The effects of human impacts in marine environments may be first manifest in alterations to recruitment, which also constitutes the only path by which many populations could recover.
Fisheries science has long been concerned with the recruitment dynamics of fish and shellfish’. The Peter Fairweather is at the Graduate School of the Environment, Macquarie University, N S W 2109, Australia.
60
need to study the levels and variability of recruitment of all types of marine organism, as well as the distribution and abundance of adults, has recentiy been re-emphasized2,3. The stages studied (which I shall call ‘propagules’) include gametes, fertilized eggs, larvae, spores and presettlement juveniles during their production, dispersal, metamorphosis and recruitment to adult populations. Many propagules are small and undergo a planktonic phase that can be difficult to study2 and so are often ignored. Recruitment is necessary to maintain many marine populations, but how recruitment translates to subsequent abundances of adults is not fully understood. The study of such phenomena has been termed ‘recruitment processes’ in fisheries and, more recently, ‘supply-side’ ecology4,5. % 3
1991
Erde in bkophysiologischer Betrachtung: /I Die gemdssigten und arktischen Zonen, Gustav Fischer 25 Gimingham, C.H. (1972) Ecology of Heath/an&, Chapman 81 Hall 26 Power, M.E. (1985) Ecology 66, 1448-I 456 27 Polis, G.A., Myers, CA. and Holt, R. (1989) Annu. Rev. Ecol. Syst. 20, 297-330 28 Pimm, S.L. (1982) Food Webs, Chapman & Hail 29 Stein, R.A. et al. (1988) in Complex interactions in Lake Communities (Carpenter, S.R., ed.), pp. 161-179, Springer-Verlag 30 Cousins, S. (1990) Oikos 57, 370-375 31 Vadas, R.L., Jr (1990) Environ. Biol. Fish. 27, 285-302 32 Polis, G.A. Am. Nat. (in press) 33 Rhoades, D.F. (1985) Am. Nat. 125, 205-238 34 Haukioja, E. and Niemeld, P. (1979) Oecologia 39, 151-I 59 35 Abrams, P.A. (1984) Am. Nat. 124, 80-96 36 Ulanowicz, R.E. and Puccia, C.J. (1990) Coenoses 5, 7-16 37 Ulanowicz, R.E. (1989) in Towards a More Exact Ecology (Grubb, P.J. and Whittaker, R.H.), pp. 327-351, Blackwell 38 Cousins, S.H. (1980) J. Theor. Biol. 82, 607-618 39 Menge, B.A. and Sutherland, J.P. (1987) Am. Nat. 130,730-757
‘Supply-side’ ecology has so far included studies of the physical transport of propagules, the role of recruitment limitation or variability in determining population levels and as input to interactions within assemblages2, as well as biogeographic scales of dispersal over ecological or evolutionary time scales4. The extent of this domain was only vaguely specified by Roughgarden and others’, who coined the term, and by Lewin5, who popularized it. The term itself has been criticized as a neologism2,“and as representing a bandwagon’. More substantial criticism’” has revolved around the fact that papers developing these principles have concentrated on species, such as barnacles, that have very long larval lives and thus much potential for variability in recruitment. Species with shorter periods in the plankton, such as algae and many colonial animals may engage in less dispersal and consequently have much tighter stock-recruitment relationships7,8. Nevertheless, longer larval durations are widespread” amongst marine taxa such as fish, molluscs, crustaceans, echinoderms
TREE vol. 6, no. 2, February
1991 ADULT STOCK
and polychaetes. We need to establish whether short larval lives and dispersal are really associated with a modular lifestyle in subtidal habitats and, conversely, long-range dispersal with solitary organisms living in intertidal or temporary habitats. The implications of recruitment variability and the consequences of these processes for environmental assessment and management have rarely been examined beyond the realm of the fisheries literature (see, for example, Ref. I I. My concern here is with environmental impact assessment and monitoring, rather than resource management as done in fisheries science. Environmental research often neglects the early stages of an organism’s life history (and thus parallels much ecological research2), yet these may also be affected by human actions. A first step in reversing this trend is to recognize that recruitment processes are important in some habitats, and in ways that can affect the assessment of environmental impacts. Once recognized, these insights can be incorporated into assessment and monitoring methodologies Here I draw together mainstream ecological research (mainly from the Southern Hemisphere) indirectly pertaining to the question of how knowledge of ‘supply-side’ concepts can aid us in management decisions. Few of the authors cited here wrote for an audience of environmental managers, yet the results they produced are clearly relevant to the aims of informed management. This is a good example of basic research yielding much when applied to problems of a managerial nature. Stock-recruitment relationships Understanding the relationship between an exploited or fishable stock and the likely recruitment to it in subsequent years has long been the cornerstone of attempts to set harvest levels in traditional fisheries management’~‘,“. There is a vast literature emanating from fisheries science on this topic (see, for example, Refs I, 61, but recent developments have obviously increased the sophistication of the statistical and theoretical models used to estimate this relationship for a given fishery.
A major conceptual advance concerns the circuit of migrationlo common to many commercially fished species, which spatially distinguished spawning grounds, nursery areas and adult stocks (Fig. I I. The first two are linked by the denatant drift of propagules, and the process of recruitment to the stock occurs when juvenile fish leave the nursery to join the adults. The distinction of three life phases is a concept useful to our thinking about ‘supply-side’ ecology even in the absence of geographical separation, and may explain why many of the impacts involving ‘supply-side’ ecology have been surprising or unforeseen (see belowl. Transport processes in the dispersal of propagules The means by which long-lived larvae and other propagules disperse to nursery areas usually involve some passive phase of movement via oceanic and/or estuarine currents. The net displacement in such cases will often be downstream or out to sea, which is, by definition, away from any coastal habitat of adults. Scientists have long puzzled over the means by which particular species can return to adult stock areas”. We now know that this occurs by a combination of oceanographic features and larval behavior12. Some larvae (such as those of crabs’3) are carried by currents into and out of estuaries via taxes involving control of buoyancy and selection of water masses moving in different directions. At the more passive end of this spectrum, we now know that plankton (including larvae and juvenile fish) and other drift material are concentrated in oceanographic features called ‘slicks’i2~‘4~15. These are associated with internal waves propagated by circulating cells of water (see Ref. I4 for an illustration I or tidal changes12, and can be generated by water flow around headlands, oceanic fronts, thermoclines, etc. Larvae are entrained in such slicks as passive particlesI and, in the case of tidal slicks, these proceed onto the coast as the tide recedes14. Any disruption to (or change in direction of) the currents, slicks or other oceanographic features could endanger the return of propagules
GROUND
Dispersal
Fig. I. The circuit of migration for many commercially harvested fish species, which may also apply to other fish and invertebrates in oceans iand estuaries. Modified after Ref IO.
to nursery areas. This may be of particular concern when considering ramifications of the Greenhouse Effect. Currents that have long supplied larvae for stocks of commercial or other interest (e.g. the Leeuwin Current off Western Australia16) may well be altered by the predicted changes to weather patterns or rise in sea level. We also need to evaluate the environmental implications of all engineering works that may disrupt currents (e.g. dredging, or constructing a breakwater or a causeway) from this perspective. At least one decline in a stock of lobsters has been attributed in part to such a change: closure of the Strait of Canso in Canada” disrupted migration of larval lobsters to the adult stocks off Nova Scotia. Natural features such as offshore kelp beds or coral reefs can act as ‘filters”8,‘9, removing organisms like larval barnacles on their way to seashores. Human actions that either promote or remove kelp beds may thus decrease or increase, respectively, the realized intensity of settlement and subsequent recruitment of populations of marine organisms in a different habitat and some distance away’“. This suggests that site-specific assessments of the environmental impact of changes to a kelp bed will overlook effects of this nature, especially beyond the boundary of the bed. Destinations of propagules The nursery areas for which marine larvae are bound are often particular settling-site habitats. For example, many species of fish and crustaceans seem to settle and metamorphose to iuvenile or postlarval stages only in seagrass meadows. In the culmination of a 61
TREE vol. 6, no. 2, February
series of studies, Bell and others20 used natural seagrass areas and smaller artificial seagrass patches to examine experimentally the recruitment of 98 species in an Australian estuary. They found that seagrass patches in every location acted as significant collectors of recruiting organisms, and that different species recruited into different parts of the estuary. They concluded that seagrass meadows in all parts of an estuary are used as nursery sites, and that conservation measures should include as many patches in as many different locations as possible within any estuary, to cater for all species*O. More recent work in the USA*’ has also suggested that proximity to large stands of seagrass or to the open sea can be used to predict the level of recruitment that any given patch of seagrass may experience. Thus we are alerted to the importance of keeping an array of seagrass in a variety of locations, including a complete size range of patches. These studies also suggest that, if natural seagrass is not available or declines, we may be able to use artificial seagrass (or other forms of shelter) to encourage recruitment. Requirements of species beyond the recruiting stage need further study. Habitats as nurseries The types of habitat required as nurseries, and particularly their role in providing shelter and food, are also important. Several recent studies (largely from Australia, South Africa and New Zealand) have emphasized that nurseries are often located in nearshore waters22. For example, dense assemblages of larval, recruiting or juvenile fish have been discovered in seagrass meadows20,2’, creeks through saltmarshes and mangroves23, the surf zone of sandy beaches22,24, inshore kelp beds25,2b, inshore gullies27 and rocky reefs**, and amongst algal wrack drifting offshore29 or inshore along beaches30. These concentrations of fish and other organisms suggest important roles for such habitats as propagule destinations, larval attractors and nursery areas. Any human use that degrades the value of these habitats as nurseries presents a major risk to resident populations. Of particular concern is
the discharge of sewage or industrial effluents at shoreline outfalls; these pollutants may also passively accumulate in slicks. For example, the release of chlorate from pulp mills in the Baltic Sea has been blamed26 for the dramatic decline of large brown algae, from being the dominant benthos to very sparse standing stocks. Kelps are extremely susceptible to chlorate and this, in turn, has been blamed for losses of fish stocks (including pelagic species), because these fish use the macroalgae to shelter and feed in during their early lives26. Such indirect and wide-reaching impacts should be considered in environmental assessments of any coastal development. Environmental monitoring An awareness of ‘supply-side’ ecology can also be useful, in at least two ways, for programs monitoring degradation of the environment. First, the ‘diminishment3’ or alteration of recruitment may be the first indication of a pollution event or other environmental hazard. This is because of the sensitivity of larvae to settling cues from altered substrata or to direct damage that may be sublethal to adult organisms, as well as the disruption of the mechanisms of transport, settlement and development outlined above. To focus only upon adult organisms may be to miss important changes*. A recent call to assess sealevel rise by monitoring intertidal organisms3* relies in part on detecting changes in the vertical level of recruitment to populations as an early warning of increasing sea level. This is particularly important for long-lived organisms, which may not be able to respond to changing conditions Analysis of the newest arrivals may reveal a more current picture of environmental conditions, provided we can separate such changes from the inherent variability in recruitment. Thus, recruitment phenomena present both an opportunity to gain early warning of environmental deterioration and a hindrance to detecting such changes (because of the ‘noisiness’ of recruitment’,2). Only elaborate, well-replicated sampling schemes providing lengthy time-series of data can overcome this dilemma. Second, recruitment is often
1991
the only available mode of recolonization of affected areas after an environmental impact. This is especially so where the impact is severe, removing all existing organisms (even those that can reproduce clonally). Thus, careful monitoring of recruitment is needed to gauge the potential for recovery, over and above the natural variability. Measuring only the adult stages of organisms cannot distinguish between difficulties with recruitment and problems with continued survival*. These alternatives need to be distinguished to plan for the rehabilitation of any impacted site. Marine reserve design ‘Supply-side’ ecology also has implications for protecting marine and estuarine areas. The scale of realized dispersal and larval connectedness among coral reefs3’, for example, helps define the units to be managed. The discussion above indicates that reserved areas with seagrass or macroalgae can act as ‘keystone’ habitats by providing the conditions for continued recruitment In addition, there is recent evidence that marine reserves may contribute to increased catches of fishery species beyond their boundaries3”, because protected areas may export propagules to other locations that are in fact acting as population sinksj5. This suggests that areas that produce large numbers of propagules should be included within reserves: this might ensure a supply of settlers and thus the continued seeding of larger areas of coast by relatively small reserves3”. Commercial or recreational fishing stocks may also benefit. Testing such a proposition requires the daunting task of assessing the source of reliably abundant standing crops of recruits; this may become easier in the future with advances in DNA fingerprinting and other genetic marker techniques The above discussion indicates how research on early life stages of marine organisms can help us to identify the impacts that we need to t II understand, (21 be able to assess, and (31 control, in order to manage environmental issues appropriately. These conclusions reaffirm and extend basic insights that originated in fisheries science
TREE vol. 6, no. 2, February
1991
The meaning and domain of ‘supply-side’ ecology Neologisms such as ‘supply-side’ can be unnecessary or confusing, but are warranted when they either focus attention upon an important issue (e.g. Hurlbert’s use of ‘pseudoreplication’37) or gather together several logically related but previously isolated concepts. Although I concentrate above on examples from marine and estuarine habitats (for which the concepts of ‘supply-side’ ecology are best developedl, the general principles of these arguments may be applicable in many other ecosystems. Such concepts are broadly analogous to terrestrial phenomena such as the dispersal of pollen or seeds, establishment of seedlings, ballooning of spiderlings, macroinvertebrate drift in communities, philopatric dispersal of prereproductive vertebrates, and probably other ecological phenomenas5. Terms like ‘recruitment variation or limitation’9 and ‘dispersal’ reflect only parts of this propagulethrough-young-stage syndrome. To draw such analogies might bring together disparate branches of ecology. For pollen3s, seeds39,40 and drift in streams4’ there exist cases of environmental implications similar to those for the marine examples discussed above. There is also the issue of the logical primacy of ‘supply-side’ concepts. As shown by Krebs42, organisms must disperse to, and select habitats in, new locations before they can be affected by the physico-chemical and biotic environments there. This suggests that ‘supply-side’ concepts may invoke simpler processes (similar to ideas of vicariance, passive dispersal and passive habitat selection in biogeography43I to explain observed phenomena. For example, it is possible that geometric speciesabundance curves of ant assembIages44 might be explained by a range of propensities of ant species to move nests and so pre-empt each other (without reference to resource levels). This alternative, ‘supplyside’, explanation does not invoke competitive mechanisms but will lead to further research (e.g. on the patterns and causes of ant colony movements). If these analogies hold. then environmental assess-
ment in terrestrial habitats will also benefit from consideration of ‘supply-side’ ecology. We should attempt to define all new technical terms in a rigorous manner. I see the domain of ‘supplyside’ ecology as including all phenomena to do with the early stages and movements of organisms. Thus, the number of propagules produced, their dispersal, their settlement, metamorphosis or germination, their early postsettlement mortality, establishment or ecesis, and their recruitment all fall under this rubric. These different stages can be viewed as a series of thresholds or filters through which individual organisms must pass to reach the adult stage (and thus contribute to the population). Early life history forms an important part of the dynamics of a population and is as worthy of study as any other aspect of an organism’s biology. Acknowledgements This work was supported by the Australian Research Council and Macquarie University Research Grants. N. Babicka drew the figure. The manuscript benefited greatly from discussions with, and the comments of, A. Beattie, I. Bell, M. Keough, M Kingsford, P. Petraitis, I. Pickard, C. Quinn, D. Stewart, A. Underwood, M. Westoby and two referees.
References I Sissenwine, M.P., Fogarty. M.j. and Overholtz, W.J. (19881 in Fish Population Dynamics: The Implications for Management (2nd ednl IGulland, J.A., ed.1, pp. 129-152, John Wiley & Sons 2 Underwood, A.f. and Fairweather. P.G ( I9891 Trends Ecol. Evol. 4, 16-20 3 Safe, P.F. ( 19901 Trends Eco/. Evol. 5, 25-27 4 Roughgarden, J., Gaines, S.D. and Pacala. S.W. ( 19871 in Organization of Communities (Gee, I.H.R. and Gilder, P.S., edsl, pp. 49 l-5 18, Blackwell 5 Lewin, R. f 19871 Science 234, 25-27 6 Young,C.M.119871Science235,415-416 7 Keough, M.I. f 19881 Proc. 6th Int. Coral ReefSymp. I, 141-148 8 Butler, A.I. and Keough. M.I. ( 1990) Trends Ecol. Evol. 5,97 9 Karlson, R.H. and Levitan, D.R. t 1990) Oecologia 82,40-44 IO Harden-lones, F.R. (I9681 Fish Migration, Edward Arnold I I Hamner, W.M. ( 19881 Trends Ecol. Evol. 3. 116-l I8 I2 Wolanski, E. and Hamner, W.M. f 19881 Science 24 I, I 77- I8 I I3 fohnson, D.R. and Hester, B.S. II9891 Estuarine Coast. Shelf Sci. 28,459-472 I4 Shanks, A.L. and Wright, W.G. f 19871 1. Exp. Mar Bio/. Ecol. I 14, I-I 3 I5 Kingsford, M.1. and Choat, 1.H. t 1986) Mar. Biol.91. 161-171
I6 Maxwell, I.C.H. and Cresswell. G.R. t 19811 Aust. 1. Mar. Freshwater Res. 32, 493-500 17 Harding, G.C., Drinkwater, K.F. and Vass, W.P. (19831 Can. 1. Fish. Aquat Sci. 40, 168-184 I8 Dayton, P.K. and Tegner, M.I. t I9841 in A New Ecology (Price, P.W.. Slobodchikoff, C.N. and Gaud, W.S.. edsl, pp. 457-481. Wiley-Interscience I9 Gaines, S.D. and Roughgarden, f. t 19871 Science 235, 479-481 20 Bell, I.D.. Steffe, A.S. and Westoby, M. ( I9881 1. Exp. Mar. Biol. Ecol. 122, 127-l 46 21 Sogard, SM. ( 19891 /. Exp. Mar. Bio/. Eco/. 133, 15-37 22 Bennett, B.A. ( 19891 Estuarine Coast. Shelf Sci. 28, 293-305 23 Morton, R.M., Pollock, B.R and Beumer, I.P. (I9871 Aust. 1. Eco/. 12, 217-237 24 Whitfield, A.K. ( 19891 Estuarine Coast. Shelf Sci. 29, 533-547 25 Carr, M.H. ( 19891 j. Exp. Mar. Biol. Ecol. 126, 59-76 26 Lehtinen, K., Notini, M., Mattsson, I. and Landner. L. ( 19881 Ambio 17, 387.-393 27 Smale, MJ. and Buxton, C D ( 19891 S. Afr. I. Zool. 24, 58-67 28 Kingsford, M.J. and Choat, 1.H. f 1989) Mar. Biol. IO I, 285-297 29 Kingsford, M.J. and Choat, I H. 11985) Urnno/. Oceanogr. 30.6 18-630 30 Lenanton, R.C.I. and Caputi, N (19891 1. Exp. Mar. Biol. Ecol. 128, I65- I78 31 Menzie. C.A. ( I9841 Mar. PO//IL Bull. 15, 127-128 32 Bird, E.C.F. (19881 in Greenhouse Planning for Climate Change 1 Pearman. C I., ed.). pp. 60-73, CSIRO, Australia 33 Sammarco, PW. and Andrews. I.C f 19881 Science 239, 1422-l 424 34 Davis, G.E. and Dodrill, I W l1’389) Bull. Mar. Sci. 44, 78-88 35 Puffiam, H.R. f 19881 A m Nat 132, 652-661 36 Cairns, D.K. and Elliot, R.D. II9871 Biol. Conserv 40, l-9 37 Hurlbert, S.I. I I9841 Eco/. Monogr 54, 187-21 I 38 McClanahan, T.R. (19861 Environ. Manage. IO. 38 l-383 39 Howe, H.F. II9841 Biol. Conseni 30. 261-281 40 Willson, M.F. and Crome, F.I. II9891 1. Trop. &co/. 5, 30 l-308 41 Townsend, C.R. (1989) I. N. A m Benthol. Sot. 8, 36-50 42 Krebs, C.1. (1985) Ecology (3rd edn), Harper & Row 43 McGuinness, K.A. f 19841 / Biogeogr. I Ia 439-456 44 Herbers, f.M. f 19891 Oecologia 81, 201-21 I
In the previous issue (7REE January 1991, p. 31), the author of a Latter on demographic growth analysis was incorrectly given as J. M ichael W&s rather than I. M ichael Weis. We apologize for this error.
63
even internally - fortunately, one might say. Differences on the level of specific issues stimulate theoretical analyses, comparative empirical studies and experiments, and thus serve as fuel for scientific progress. Acknowledgements Sincerest thanks to Stephen Cousins, Lennart Persson, Stuart P i m m and Robert Vadas for constructive critiques, clarifications of their viewpoints and for suggestions of useful references.
References 1 Patten, B.C. and Odum, E.P. (1981) Am. Nat. 118.886-895 2 Odum; E.P. and Biever, L.J. (1984) Am. Nat. 124,360-376 3 Cousins. S. (1987) Trends Ecol. Evol. 2. 312-316 4 Vadas, R.L., Jr (1989) Oikos 56, 339-343 5 Oksanen, L. (1988) Am. Nat. 131, 424-444 6 Odum, E.P. (1971) Fundamentals of Ecology (3rd edn), W.B. Saunders 7 Odum. H.T. 11960) Am. SC;. 48, l-8 8 Odum, H.T. (1971) Environment, Power and Society, Wiley & Sons 9 Ulanowicz, R.E. (1990) Oikos 57,42-48 IO Hairston, N.G., Smith, F.E. and
Slobodkin, L.B. (1960) Am. Nat. 94, 421-425 11 Slobodkin, L.B., Smith, F.E. and Hairston, N.C. (1967) Am. Nat 101, 109-124 12 Fretwell, S.D. (1977) Perspect. Biol. Med. 20, ‘I69-l 85 13 Oksanen, L., Fretwell, SD., Arruda, J. and Niemela, P. (1981) Am. Nat. 118, 240-261 14 Fretwell, S.D. (1987) Oikos 50, 291-301 15 Oksanen, L. and Ericson, L. (1987) Oikos 50,417-422 16 Oksanen, L. (1990) Oikos 57, 14-24 17 Oksanen, T. (1990) Evol. Ecol. 4, 220-234 18 Persson, L., Andersson, G., Hamrin, S.F. and Johansson, L. (1988) in Complex interactions in Lake Communities (Carpenter, S.R., ed.), pp. 45-65, Springer-Verlag 19 Carpenter, S.R., Kitchell, J.F. and Hogson, J.R. (1985) Bioscience 35, 634-639 20 Murdoch, W.W. (1966) Am. Nat. 100, 219-226 21 Ehrlich, P.R. and Birch, L.C. (1967) Am. Nat. 101,97-107 22 Schoener, T.W. (1983) Am. Nat. 122, 240-285 23 Schoener, T.W. (1985) Am. Nat. 125, 730-740 24 Walter, H. (1968) Die Vegetation der
implications of ‘Supply-side’ Ecologyfor Envirorkhtal Assessment andManagement PeterG, Fairweather Recent work iti marine ecology has reaffirmed UM insight from fisheries science that knowledge about the production, dissemination and success of propagules can guide our management of populations and assemblages. Understanding the variable nature
of recruitment
rebtionships
can
both aid and hinder attempts at environmental monitoring, rehabilitation and innovative selection of marine reserves. The effects of human impacts in marine environments may be first manifest in alterations to recruitment, which also constitutes the only path by which many populations could recover.
Fisheries science has long been concerned with the recruitment dynamics of fish and shellfish’. The Peter Fairweather is at the Graduate School of the Environment, Macquarie University, N S W 2109, Australia.
60
need to study the levels and variability of recruitment of all types of marine organism, as well as the distribution and abundance of adults, has recentiy been re-emphasized2,3. The stages studied (which I shall call ‘propagules’) include gametes, fertilized eggs, larvae, spores and presettlement juveniles during their production, dispersal, metamorphosis and recruitment to adult populations. Many propagules are small and undergo a planktonic phase that can be difficult to study2 and so are often ignored. Recruitment is necessary to maintain many marine populations, but how recruitment translates to subsequent abundances of adults is not fully understood. The study of such phenomena has been termed ‘recruitment processes’ in fisheries and, more recently, ‘supply-side’ ecology4,5. % 3
1991
Erde in bkophysiologischer Betrachtung: /I Die gemdssigten und arktischen Zonen, Gustav Fischer 25 Gimingham, C.H. (1972) Ecology of Heath/an&, Chapman 81 Hall 26 Power, M.E. (1985) Ecology 66, 1448-I 456 27 Polis, G.A., Myers, CA. and Holt, R. (1989) Annu. Rev. Ecol. Syst. 20, 297-330 28 Pimm, S.L. (1982) Food Webs, Chapman & Hail 29 Stein, R.A. et al. (1988) in Complex interactions in Lake Communities (Carpenter, S.R., ed.), pp. 161-179, Springer-Verlag 30 Cousins, S. (1990) Oikos 57, 370-375 31 Vadas, R.L., Jr (1990) Environ. Biol. Fish. 27, 285-302 32 Polis, G.A. Am. Nat. (in press) 33 Rhoades, D.F. (1985) Am. Nat. 125, 205-238 34 Haukioja, E. and Niemeld, P. (1979) Oecologia 39, 151-I 59 35 Abrams, P.A. (1984) Am. Nat. 124, 80-96 36 Ulanowicz, R.E. and Puccia, C.J. (1990) Coenoses 5, 7-16 37 Ulanowicz, R.E. (1989) in Towards a More Exact Ecology (Grubb, P.J. and Whittaker, R.H.), pp. 327-351, Blackwell 38 Cousins, S.H. (1980) J. Theor. Biol. 82, 607-618 39 Menge, B.A. and Sutherland, J.P. (1987) Am. Nat. 130,730-757
‘Supply-side’ ecology has so far included studies of the physical transport of propagules, the role of recruitment limitation or variability in determining population levels and as input to interactions within assemblages2, as well as biogeographic scales of dispersal over ecological or evolutionary time scales4. The extent of this domain was only vaguely specified by Roughgarden and others’, who coined the term, and by Lewin5, who popularized it. The term itself has been criticized as a neologism2,“and as representing a bandwagon’. More substantial criticism’” has revolved around the fact that papers developing these principles have concentrated on species, such as barnacles, that have very long larval lives and thus much potential for variability in recruitment. Species with shorter periods in the plankton, such as algae and many colonial animals may engage in less dispersal and consequently have much tighter stock-recruitment relationships7,8. Nevertheless, longer larval durations are widespread” amongst marine taxa such as fish, molluscs, crustaceans, echinoderms
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1991 ADULT STOCK
and polychaetes. We need to establish whether short larval lives and dispersal are really associated with a modular lifestyle in subtidal habitats and, conversely, long-range dispersal with solitary organisms living in intertidal or temporary habitats. The implications of recruitment variability and the consequences of these processes for environmental assessment and management have rarely been examined beyond the realm of the fisheries literature (see, for example, Ref. I I. My concern here is with environmental impact assessment and monitoring, rather than resource management as done in fisheries science. Environmental research often neglects the early stages of an organism’s life history (and thus parallels much ecological research2), yet these may also be affected by human actions. A first step in reversing this trend is to recognize that recruitment processes are important in some habitats, and in ways that can affect the assessment of environmental impacts. Once recognized, these insights can be incorporated into assessment and monitoring methodologies Here I draw together mainstream ecological research (mainly from the Southern Hemisphere) indirectly pertaining to the question of how knowledge of ‘supply-side’ concepts can aid us in management decisions. Few of the authors cited here wrote for an audience of environmental managers, yet the results they produced are clearly relevant to the aims of informed management. This is a good example of basic research yielding much when applied to problems of a managerial nature. Stock-recruitment relationships Understanding the relationship between an exploited or fishable stock and the likely recruitment to it in subsequent years has long been the cornerstone of attempts to set harvest levels in traditional fisheries management’~‘,“. There is a vast literature emanating from fisheries science on this topic (see, for example, Refs I, 61, but recent developments have obviously increased the sophistication of the statistical and theoretical models used to estimate this relationship for a given fishery.
A major conceptual advance concerns the circuit of migrationlo common to many commercially fished species, which spatially distinguished spawning grounds, nursery areas and adult stocks (Fig. I I. The first two are linked by the denatant drift of propagules, and the process of recruitment to the stock occurs when juvenile fish leave the nursery to join the adults. The distinction of three life phases is a concept useful to our thinking about ‘supply-side’ ecology even in the absence of geographical separation, and may explain why many of the impacts involving ‘supply-side’ ecology have been surprising or unforeseen (see belowl. Transport processes in the dispersal of propagules The means by which long-lived larvae and other propagules disperse to nursery areas usually involve some passive phase of movement via oceanic and/or estuarine currents. The net displacement in such cases will often be downstream or out to sea, which is, by definition, away from any coastal habitat of adults. Scientists have long puzzled over the means by which particular species can return to adult stock areas”. We now know that this occurs by a combination of oceanographic features and larval behavior12. Some larvae (such as those of crabs’3) are carried by currents into and out of estuaries via taxes involving control of buoyancy and selection of water masses moving in different directions. At the more passive end of this spectrum, we now know that plankton (including larvae and juvenile fish) and other drift material are concentrated in oceanographic features called ‘slicks’i2~‘4~15. These are associated with internal waves propagated by circulating cells of water (see Ref. I4 for an illustration I or tidal changes12, and can be generated by water flow around headlands, oceanic fronts, thermoclines, etc. Larvae are entrained in such slicks as passive particlesI and, in the case of tidal slicks, these proceed onto the coast as the tide recedes14. Any disruption to (or change in direction of) the currents, slicks or other oceanographic features could endanger the return of propagules
GROUND
Dispersal
Fig. I. The circuit of migration for many commercially harvested fish species, which may also apply to other fish and invertebrates in oceans iand estuaries. Modified after Ref IO.
to nursery areas. This may be of particular concern when considering ramifications of the Greenhouse Effect. Currents that have long supplied larvae for stocks of commercial or other interest (e.g. the Leeuwin Current off Western Australia16) may well be altered by the predicted changes to weather patterns or rise in sea level. We also need to evaluate the environmental implications of all engineering works that may disrupt currents (e.g. dredging, or constructing a breakwater or a causeway) from this perspective. At least one decline in a stock of lobsters has been attributed in part to such a change: closure of the Strait of Canso in Canada” disrupted migration of larval lobsters to the adult stocks off Nova Scotia. Natural features such as offshore kelp beds or coral reefs can act as ‘filters”8,‘9, removing organisms like larval barnacles on their way to seashores. Human actions that either promote or remove kelp beds may thus decrease or increase, respectively, the realized intensity of settlement and subsequent recruitment of populations of marine organisms in a different habitat and some distance away’“. This suggests that site-specific assessments of the environmental impact of changes to a kelp bed will overlook effects of this nature, especially beyond the boundary of the bed. Destinations of propagules The nursery areas for which marine larvae are bound are often particular settling-site habitats. For example, many species of fish and crustaceans seem to settle and metamorphose to iuvenile or postlarval stages only in seagrass meadows. In the culmination of a 61
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series of studies, Bell and others20 used natural seagrass areas and smaller artificial seagrass patches to examine experimentally the recruitment of 98 species in an Australian estuary. They found that seagrass patches in every location acted as significant collectors of recruiting organisms, and that different species recruited into different parts of the estuary. They concluded that seagrass meadows in all parts of an estuary are used as nursery sites, and that conservation measures should include as many patches in as many different locations as possible within any estuary, to cater for all species*O. More recent work in the USA*’ has also suggested that proximity to large stands of seagrass or to the open sea can be used to predict the level of recruitment that any given patch of seagrass may experience. Thus we are alerted to the importance of keeping an array of seagrass in a variety of locations, including a complete size range of patches. These studies also suggest that, if natural seagrass is not available or declines, we may be able to use artificial seagrass (or other forms of shelter) to encourage recruitment. Requirements of species beyond the recruiting stage need further study. Habitats as nurseries The types of habitat required as nurseries, and particularly their role in providing shelter and food, are also important. Several recent studies (largely from Australia, South Africa and New Zealand) have emphasized that nurseries are often located in nearshore waters22. For example, dense assemblages of larval, recruiting or juvenile fish have been discovered in seagrass meadows20,2’, creeks through saltmarshes and mangroves23, the surf zone of sandy beaches22,24, inshore kelp beds25,2b, inshore gullies27 and rocky reefs**, and amongst algal wrack drifting offshore29 or inshore along beaches30. These concentrations of fish and other organisms suggest important roles for such habitats as propagule destinations, larval attractors and nursery areas. Any human use that degrades the value of these habitats as nurseries presents a major risk to resident populations. Of particular concern is
the discharge of sewage or industrial effluents at shoreline outfalls; these pollutants may also passively accumulate in slicks. For example, the release of chlorate from pulp mills in the Baltic Sea has been blamed26 for the dramatic decline of large brown algae, from being the dominant benthos to very sparse standing stocks. Kelps are extremely susceptible to chlorate and this, in turn, has been blamed for losses of fish stocks (including pelagic species), because these fish use the macroalgae to shelter and feed in during their early lives26. Such indirect and wide-reaching impacts should be considered in environmental assessments of any coastal development. Environmental monitoring An awareness of ‘supply-side’ ecology can also be useful, in at least two ways, for programs monitoring degradation of the environment. First, the ‘diminishment3’ or alteration of recruitment may be the first indication of a pollution event or other environmental hazard. This is because of the sensitivity of larvae to settling cues from altered substrata or to direct damage that may be sublethal to adult organisms, as well as the disruption of the mechanisms of transport, settlement and development outlined above. To focus only upon adult organisms may be to miss important changes*. A recent call to assess sealevel rise by monitoring intertidal organisms3* relies in part on detecting changes in the vertical level of recruitment to populations as an early warning of increasing sea level. This is particularly important for long-lived organisms, which may not be able to respond to changing conditions Analysis of the newest arrivals may reveal a more current picture of environmental conditions, provided we can separate such changes from the inherent variability in recruitment. Thus, recruitment phenomena present both an opportunity to gain early warning of environmental deterioration and a hindrance to detecting such changes (because of the ‘noisiness’ of recruitment’,2). Only elaborate, well-replicated sampling schemes providing lengthy time-series of data can overcome this dilemma. Second, recruitment is often
1991
the only available mode of recolonization of affected areas after an environmental impact. This is especially so where the impact is severe, removing all existing organisms (even those that can reproduce clonally). Thus, careful monitoring of recruitment is needed to gauge the potential for recovery, over and above the natural variability. Measuring only the adult stages of organisms cannot distinguish between difficulties with recruitment and problems with continued survival*. These alternatives need to be distinguished to plan for the rehabilitation of any impacted site. Marine reserve design ‘Supply-side’ ecology also has implications for protecting marine and estuarine areas. The scale of realized dispersal and larval connectedness among coral reefs3’, for example, helps define the units to be managed. The discussion above indicates that reserved areas with seagrass or macroalgae can act as ‘keystone’ habitats by providing the conditions for continued recruitment In addition, there is recent evidence that marine reserves may contribute to increased catches of fishery species beyond their boundaries3”, because protected areas may export propagules to other locations that are in fact acting as population sinksj5. This suggests that areas that produce large numbers of propagules should be included within reserves: this might ensure a supply of settlers and thus the continued seeding of larger areas of coast by relatively small reserves3”. Commercial or recreational fishing stocks may also benefit. Testing such a proposition requires the daunting task of assessing the source of reliably abundant standing crops of recruits; this may become easier in the future with advances in DNA fingerprinting and other genetic marker techniques The above discussion indicates how research on early life stages of marine organisms can help us to identify the impacts that we need to t II understand, (21 be able to assess, and (31 control, in order to manage environmental issues appropriately. These conclusions reaffirm and extend basic insights that originated in fisheries science
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The meaning and domain of ‘supply-side’ ecology Neologisms such as ‘supply-side’ can be unnecessary or confusing, but are warranted when they either focus attention upon an important issue (e.g. Hurlbert’s use of ‘pseudoreplication’37) or gather together several logically related but previously isolated concepts. Although I concentrate above on examples from marine and estuarine habitats (for which the concepts of ‘supply-side’ ecology are best developedl, the general principles of these arguments may be applicable in many other ecosystems. Such concepts are broadly analogous to terrestrial phenomena such as the dispersal of pollen or seeds, establishment of seedlings, ballooning of spiderlings, macroinvertebrate drift in communities, philopatric dispersal of prereproductive vertebrates, and probably other ecological phenomenas5. Terms like ‘recruitment variation or limitation’9 and ‘dispersal’ reflect only parts of this propagulethrough-young-stage syndrome. To draw such analogies might bring together disparate branches of ecology. For pollen3s, seeds39,40 and drift in streams4’ there exist cases of environmental implications similar to those for the marine examples discussed above. There is also the issue of the logical primacy of ‘supply-side’ concepts. As shown by Krebs42, organisms must disperse to, and select habitats in, new locations before they can be affected by the physico-chemical and biotic environments there. This suggests that ‘supply-side’ concepts may invoke simpler processes (similar to ideas of vicariance, passive dispersal and passive habitat selection in biogeography43I to explain observed phenomena. For example, it is possible that geometric speciesabundance curves of ant assembIages44 might be explained by a range of propensities of ant species to move nests and so pre-empt each other (without reference to resource levels). This alternative, ‘supplyside’, explanation does not invoke competitive mechanisms but will lead to further research (e.g. on the patterns and causes of ant colony movements). If these analogies hold. then environmental assess-
ment in terrestrial habitats will also benefit from consideration of ‘supply-side’ ecology. We should attempt to define all new technical terms in a rigorous manner. I see the domain of ‘supplyside’ ecology as including all phenomena to do with the early stages and movements of organisms. Thus, the number of propagules produced, their dispersal, their settlement, metamorphosis or germination, their early postsettlement mortality, establishment or ecesis, and their recruitment all fall under this rubric. These different stages can be viewed as a series of thresholds or filters through which individual organisms must pass to reach the adult stage (and thus contribute to the population). Early life history forms an important part of the dynamics of a population and is as worthy of study as any other aspect of an organism’s biology. Acknowledgements This work was supported by the Australian Research Council and Macquarie University Research Grants. N. Babicka drew the figure. The manuscript benefited greatly from discussions with, and the comments of, A. Beattie, I. Bell, M. Keough, M Kingsford, P. Petraitis, I. Pickard, C. Quinn, D. Stewart, A. Underwood, M. Westoby and two referees.
References I Sissenwine, M.P., Fogarty. M.j. and Overholtz, W.J. (19881 in Fish Population Dynamics: The Implications for Management (2nd ednl IGulland, J.A., ed.1, pp. 129-152, John Wiley & Sons 2 Underwood, A.f. and Fairweather. P.G ( I9891 Trends Ecol. Evol. 4, 16-20 3 Safe, P.F. ( 19901 Trends Eco/. Evol. 5, 25-27 4 Roughgarden, J., Gaines, S.D. and Pacala. S.W. ( 19871 in Organization of Communities (Gee, I.H.R. and Gilder, P.S., edsl, pp. 49 l-5 18, Blackwell 5 Lewin, R. f 19871 Science 234, 25-27 6 Young,C.M.119871Science235,415-416 7 Keough, M.I. f 19881 Proc. 6th Int. Coral ReefSymp. I, 141-148 8 Butler, A.I. and Keough. M.I. ( 1990) Trends Ecol. Evol. 5,97 9 Karlson, R.H. and Levitan, D.R. t 1990) Oecologia 82,40-44 IO Harden-lones, F.R. (I9681 Fish Migration, Edward Arnold I I Hamner, W.M. ( 19881 Trends Ecol. Evol. 3. 116-l I8 I2 Wolanski, E. and Hamner, W.M. f 19881 Science 24 I, I 77- I8 I I3 fohnson, D.R. and Hester, B.S. II9891 Estuarine Coast. Shelf Sci. 28,459-472 I4 Shanks, A.L. and Wright, W.G. f 19871 1. Exp. Mar Bio/. Ecol. I 14, I-I 3 I5 Kingsford, M.1. and Choat, 1.H. t 1986) Mar. Biol.91. 161-171
I6 Maxwell, I.C.H. and Cresswell. G.R. t 19811 Aust. 1. Mar. Freshwater Res. 32, 493-500 17 Harding, G.C., Drinkwater, K.F. and Vass, W.P. (19831 Can. 1. Fish. Aquat Sci. 40, 168-184 I8 Dayton, P.K. and Tegner, M.I. t I9841 in A New Ecology (Price, P.W.. Slobodchikoff, C.N. and Gaud, W.S.. edsl, pp. 457-481. Wiley-Interscience I9 Gaines, S.D. and Roughgarden, f. t 19871 Science 235, 479-481 20 Bell, I.D.. Steffe, A.S. and Westoby, M. ( I9881 1. Exp. Mar. Biol. Ecol. 122, 127-l 46 21 Sogard, SM. ( 19891 /. Exp. Mar. Bio/. Eco/. 133, 15-37 22 Bennett, B.A. ( 19891 Estuarine Coast. Shelf Sci. 28, 293-305 23 Morton, R.M., Pollock, B.R and Beumer, I.P. (I9871 Aust. 1. Eco/. 12, 217-237 24 Whitfield, A.K. ( 19891 Estuarine Coast. Shelf Sci. 29, 533-547 25 Carr, M.H. ( 19891 j. Exp. Mar. Biol. Ecol. 126, 59-76 26 Lehtinen, K., Notini, M., Mattsson, I. and Landner. L. ( 19881 Ambio 17, 387.-393 27 Smale, MJ. and Buxton, C D ( 19891 S. Afr. I. Zool. 24, 58-67 28 Kingsford, M.J. and Choat, 1.H. f 1989) Mar. Biol. IO I, 285-297 29 Kingsford, M.J. and Choat, I H. 11985) Urnno/. Oceanogr. 30.6 18-630 30 Lenanton, R.C.I. and Caputi, N (19891 1. Exp. Mar. Biol. Ecol. 128, I65- I78 31 Menzie. C.A. ( I9841 Mar. PO//IL Bull. 15, 127-128 32 Bird, E.C.F. (19881 in Greenhouse Planning for Climate Change 1 Pearman. C I., ed.). pp. 60-73, CSIRO, Australia 33 Sammarco, PW. and Andrews. I.C f 19881 Science 239, 1422-l 424 34 Davis, G.E. and Dodrill, I W l1’389) Bull. Mar. Sci. 44, 78-88 35 Puffiam, H.R. f 19881 A m Nat 132, 652-661 36 Cairns, D.K. and Elliot, R.D. II9871 Biol. Conserv 40, l-9 37 Hurlbert, S.I. I I9841 Eco/. Monogr 54, 187-21 I 38 McClanahan, T.R. (19861 Environ. Manage. IO. 38 l-383 39 Howe, H.F. II9841 Biol. Conseni 30. 261-281 40 Willson, M.F. and Crome, F.I. II9891 1. Trop. &co/. 5, 30 l-308 41 Townsend, C.R. (1989) I. N. A m Benthol. Sot. 8, 36-50 42 Krebs, C.1. (1985) Ecology (3rd edn), Harper & Row 43 McGuinness, K.A. f 19841 / Biogeogr. I Ia 439-456 44 Herbers, f.M. f 19891 Oecologia 81, 201-21 I
In the previous issue (7REE January 1991, p. 31), the author of a Latter on demographic growth analysis was incorrectly given as J. M ichael W&s rather than I. M ichael Weis. We apologize for this error.
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