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Extinction, Colonization, and Metapopulations: Environmental Tracking by Rare Species C. D. THOMAS School of Biological Sciences The University of Birmingham Edghaston, Birmingham B15 2TT, England Abstract: Extinction and metapopulation theories emphasize that stochastic fluctuations in local populations cause extinction and that local extinctions generate empty habitat patches that are then available f o r recolonizatiorL Metapopulation persistence depends on the balance o f extinction and colonization in a static environment For many rare and declining specie~ I argue (1) that extinction is usually the deterministic consequence o f the local environment becoming unsuitable (through habitat loss or modification, introduction o f a predator, eta); (2) that the local environment usually remains unsuitable following local extinction, so extinctions only rarely generate empty patches o f suitable habitat; and (3) that colonization usually follows improvement o f the local environment f o r a particular species (or long-distance transfer by humans). Thus, persistence depends predominantly on whether organisms are able to track the shifting spatial mosaic o f suitable environmental conditions or on maintainance o f good conditions locally. Extinction Over the past 20 years, extinction models have b e e n applied increasingly to populations of endangered species. Typically, an estimate is made of the median ( o r m a x i m u m ) population size that could be sustained in a Paper submitted July 17, 1993; revised manuscript accepted October 13, 199~ Extinci6n, colonizaci6n y metapoblaciones: adecuaci6n ambiental de especies raras Resumen: Las teorias sobre exttnci6n y metapoblaciones enfatizan que ftuctuaciones estocdsttcas en poblaciones locales causan la extinci6n y que la extinci6n total genera parches de hdbitat vacios que estdn entonces disponthles para la recolonizaci6rL En un ambiente estdtico, la persistencla de la metapoblaci6n depende del balance entre extinclones y colonizacionex Yo sostengo que para muchas especies raras y e n declinaci6n, (t) usualmente la extinci6n es una consecuencia deterministica de un ambiente local que se hace inadecuado (e.g., pddtda o modificaci6n del hdbita~ introducci6n de un predador, eta); (ii) usualment¢ el ambiente local permanece inadecuado It,ego de la extinct6n local p o r consiguient¢ s61o rarament¢ extinciones locales generan parches vacios de habitats adecuados; y (ii 0 usualmente la colonizacion viene despu~s de la mejora de las condiciones ambientales para una especie en particular (o la transferencla a larga dtstancla p o r humanos). Por consiguiente, la persistencia depende predominantemente de que los organismos puedan adaptarse al mosaico espacial cambiante de las condiciones ambientales o de que se mantengan buenas condiciones localex reserve, and the probability of persistence is calculated by adding stochastic variation to birth and death, either separately or combined. Variation is usefully divided into demographic stochasticity that affects the chance birth and death events of individuals independently, environmental stochasticity that affects average birth and death rates in each generation, and environmental catastrophe that can result in extinction regardless of initial population size (May 1973; Shaffer 1981). Genetic stochasticity and feedback into the population parameters may also be important. The combination of relatively small population size and stochastic variability un373 ConservationBiology,Pages373-378 Volume8, No. 2, June 1994 374 F~vironmenmlTracing by Rare Species Thomas derpinned almost all extinction models of the 1970s and 1980s (see Richter-Dyn & Goel 1972; Leigh 1981; Shaffer & Samson 1985; Strebel 1985). In most of these extinction models, mean birth and death rates w e r e assumed to be equal in the long term, even if stochasticity varied the rates from generation to generation. The models generated a decreasing probability of extinction with increasing population size, so the object of conservation was to prevent stochastic local extinction by achieving a minimum viable population size. Estimates of m i n i m u m viable population size w e r e often so large that few if any remnant populations w e r e considered large enough to be viable, at least for large terrestrial vertebrates. The objective of a new approach to extinction models is to balance stochastic local extinctions by recolonization, usually through multiple reserves and corridors (see Boyce 1992; Nunn e y & Campbell 1993). But do stochastic causes of extinction really merit the attention they have b e e n given? If direct or indirect modification of the environment by humans results in a mean birth rate that is persistently lower than the mean death rate, on average individuals do not replace themselves. In such cases organisms are on an inevitable, deterministic slide to extinction, the time taken to extinction depending on the initial population size and the extent to which the death rate is greater than the birth rate. Although deterministic causes of extinction have b e e n widely recognized (see Shaffer 1981; Gilpin & Soul6 1986; Simberloff 1988), particularly in empirical work, the clear emphasis of theory and reviews has b e e n on the importance of different types of stochasticity. It can be argued that simple models are not applied to real endangered populations and metapopulations, but the conceptual basis of these models pervades conservation thinking (see reviews by Boyce 1992; Nunney & Campbell 1993). The evidence from real population and species extinctions is that extinction is normally deterministic. A m a j o r r e v i e w of species extinctions ( G r o o m b r i d g e 1992) has revealed that m o s t animal extinctions are caused by direct hunting by humans, introductions of species with which the extinct species could not coexist, and loss of habitat (Table 1). "Habitat alteration" plus "natural" extinctions place a ceiling on the proportion of species extinctions in which stochastic processes could have played a significant part. This p r o p o r t i o n is about half for invertebrates and aquatic vertebrates and a quarter for terrestrial vertebrates (Table 1). In fact, stochasticity is important to far fewer species: in m a n y cases virtually the entire habitat was lost or modified, causing 100% mortality. Stochastic extinction from surviving habitat fragments is minor b.y comparison. The story is similar for population extinctions. Most extinctions of any but the smallest populations are determined by persistent changes in the local environm e n t (Harrison 1991; C.D. Thomas 1993, 1994), and large populations are not i m m u n e to these changes (J. A. Thomas 1991). For British butterflies, almost all local extinctions can be attributed to c o m p l e t e habitat loss (through, for example, agricultural conversion) or to m o r e subtle changes in the vegetation (such as short grass to slightly longer grass, resulting in the elimination of short-grass species). The latter could mistakenly be classifed as "stochastic extinction" in the absence of detailed knowledge of the precise habitat requirements of individual species. D o c u m e n t e d extinctions of local butterfly populations from nature reserves are almost always associated with clear, albeit subtle, changes in the habitat that r e m o v e conditions required by a particular species (J.A. Thomas 1991; W a r r e n 1993). Although unusual weather (temporal environmental stochasticity) has been responsible for several well-cited examples of local butterfly extinctions (see Ehrlich et al. 1980), most local extinctions appear to be deterministic responses to persistent changes in the local environm e n t (C. D. Thomas 1993, 1994). Typically, population stochasticity is important only in the last generations, w h e n the fate of a population has already b e e n sealed. With a stochastic approach based on m e a n birth and death rates being equal to one another, there is little a conservation manager can do other than ensure that the original population size is large. This may be good advice, but it does little to help managers p r e v e n t declines in the short term or establish recovery programs. With a m o r e deterministic approach, models can be used to explore ways of maximizing birth rates and minimizing death rates. A shift is n o w taking place in this d i r e c t i o n m t o w a r d models that concentrate on factors that determine population trends yet recognize that stochastic variability will be superimposed on the trend ( H o c h b e r g et al. Table 1. Causes of species extinctions (% a) (after Groombridge 1992). Invertebrates (n = 72) Aquatic Vertebrates (n = 28) Terrestrial Vertebrates (n = 111 ) Human Predation b Introduced Species Indirect Effects Habitat Alteration "Natural" Causes 16 8 30 33 37 46 1 4 1 49 50 22 1 1 0 a Percentages given have been rounded to the nearest whole number. Includes species consumed as food, exploited for other biological products, and deliberately eliminated as pests. ConservationBiology Volume 8, No. 2, June 1994 Thomas EnvirograentalTrackingby Rare Species 375 1992; Burgman et al. 1993). Starting population size needs to b e known, m e a n birth and death rates measured ( o r the net effect calculated from past changes in population size), and, if possible, the strength and type of density-dependence estimated. As with stochastic extinctions, deterministic extinctions are m o r e likely to take place in small rather than large populations because ( 1 ) for a given decline, small populations are likely to b e c o m e extinct sooner than large ones, and ( 2 ) large populations usually inhabit relatively large areas, such that local habitat deterioration will probably not affect the entire area simultaneously (C. D. Thomas 1991, 1994). Stochasticity in birth and d e a t h w i l l still play an important role and can be included, but the m e a n rates are crucial ( m e a n birth = mean death is just a special case). W h e n particular habitat components, such as predation by humans or distributions' of other species, affect m e a n birth and death rates (and also immigration and emigration), the implications of specific habitat conditions and m a n a g e m e n t can be predicted (Hochberg et al. 1992; Burgman et al. 1993). Stochastic models are likely to be important only w h e r e deterministic pressures have o c c u r r e d and have then b e e n alleviated. Conservation efforts should concentrate first on ensuring that birth exceeds or equals death and should w o r r y about stochasticity second. Provided that birth exceeds death at low population dens i t y m t h a t t h e r e is s o m e d e n s i t y - d e p e n d e n c e - - - e v e n quite small populations may survive well. unavailable for recolonization. For example, this w o u l d be the case if a species is eliminated from a patch of habitat because of vegetation succession, or if a species is eliminated from an island after the arrival of rats. The local e n v i r o n m e n t may or may not b e c o m e suitable again, depending on future events. Thus, the major process that creates e m p t y habitat in metapopulation models does not operate widely in nature. This is crucial. In m o s t metapopulation models, stable equilibria o c c u r because a stochastic increase in extinction generates an increased n u m b e r of habitat patches available for colonization, so there is a corresponding increase in colonization. If the link b e t w e e n extinction and subsequent colonization is broken, so is the basis for equilibrium. It is important, therefore, to recognize the events that p r e c e d e colonization in nature. Working with British butterflies, I have identified six general ( n o t entirely distinct) contexts in which natural colonizations are observed (Thomas 1993). Colonization and Metapopulations 2. Creation of New "Permanent" Habitat Close to Existing Populations Notwithstanding the above arguments, models and empirical observations suggest that very small populations are relatively likely to b e c o m e extinct (see Soul~ 1986; Lande 1988; Simberloff 1988; Thomas 1990; Kindvall & Ahl6n 1992), and, alas, m a n y local populations in remnant habitat fragments are and will remain small. If habitat remains suitable following local extinction, recolonization of the n o w - e m p t y habitat may replace at least some of these losses. The pessimistic view of continuing, inevitable extinctions has given way in the past five years to some degree of optimism that a balance may be reached b e t w e e n local extinctions and colonization. Metapopulation dynamics provide the theoretical basis for this optimism, and the approach is fast b e c o m i n g the n e w vogue in conservation biology (Gilpin & Hanski 1991; Harrison 1994). Harrison (1991, 1994) and Thomas ( 1 9 9 3 ) question w h e t h e r there is likely to be a balance b e t w e e n extinction and colonizations in m o s t natural systems, particularly w h e r e endangered species are concerned. If the cause of extinction is a deterministic population response to unsuitable conditions, the local habitat is likely to remain unsuitable after extinction and so be Freshly created habitats on road verges, railway embankments, and wide forest tracks (associated w i t h mechanized timber extraction) have b e e n colonized by many species of butterfly (Warren 1984; Munguira & T h o m a s 1992). Changes in the c o n d i t i o n of longestablished habitats have also b e e n exploited by butterflies. Rabbit grazing was virtually eliminated from calcareous grasslands in Britain following the introduction of the disease myxomatosis in the 1950s. Due to the resultant increase in long-turf habitat, one skipper butterfly, Thymelicus acteo~ colonized many n e w localities that subsequently b e c a m e dominated by its host plant (J. A. Thomas 1983). Over the same period, populations of a short-grass skipper, Hesperia c o m m ~ declined. Recovery of rabbit populations in the last 15 years has resulted in H. c o m m a colonizing at least 29 patches of grassland as new areas of short-turf habitat have b e c o m e available ( T h o m a s & Jones 1993). 1. Disturbance and Succession Following natural disturbance or h u m a n management, species colonize specific seral stages of a particular vegetation. Some generations later, they are eliminated b y succession. Examples include Mellicta athalia~ w h i c h colonizes fresh woodland clearings (Warren 1991 ), and Melitaea cinxig which colonizes crumbling cliffs (Sirecox & Thomas 1979). The dynamics of the endangered plant Pedicularisfurbishiae on river banks appear to be similar (Menges 1990). 3. Introductions Outside of Range Releasing butterflies in n e w areas, beyond their normal dispersal capacity, sometimes results in a w h o l e series of fresh colonizations. Thomas and Harrison ( 1 9 9 2 ) give Conservation Biology Volume 8, No, 2, June 1994 376 EnvironmentalTraclangby Rare Species an example. Introductions of m a n y species around the w o r l d fall into this category. 4. Increases in Range Following changes in climate or widespread changes in habitat, several sp.ecies have expanded their ranges. Ladoga camilla expanded its range in the relatively w a r m weather of the 1930s and 1940s, w h e n British woodlands b e c a m e m o r e shaded and h e n c e m o r e suitable for this species (Pollard 1979); Pyronia tithonus has expanded its range over the last 30 years (Pollard 1991). 5. Turnover-Prone Peripheral Patches In the absence of deterioration in the local environment, most extinctions are confined to the smallest habitat patches (Schoener & Spiller 1987; Harrison 1991; Schoener 1991). These patches then b e c o m e available for recolonization. Following recolonization, very small patches of habitat support short-lived local populations that are unimportant to overall persistence. A similar argument can be made for population "sinks" in p o o r habitat. 6. Seasonal Spread In fairly mobile species, a mixture of contexts four and five may be seen. Some species may survive inhospitable periods (winter, dry season) in favorable refuges (warm, mesic) and spread m o r e widely in favorable seasons (Shapiro 1979; DeVries 1987; J o r d a n o et al. 1991). Metapopulation theory is not appropriate for such mobile species. True migration is an extension of the phenomenon. These contexts share the vital condition that a species has recently c o m e into contact with favorable but unexploited environmental conditions. In most cases, previously uninhabitable localities have only recently bec o m e suitable. I am n o t a w a r e of any c o n v i n c i n g example of a local extinction that left vacant habitat that was immediately suitable for a new, viable, persistent population. Following contact, colonization is distancedependent; it is probabilistic but predictable (Thomas et al. 1992; Thomas 1993, 1994; Thomas &Jones 1993). Although the observed events preceding colonizations necessitate modification of most existing metapopulation models, there is a positive message for conservation managers. If real colonizations follow an imp r o v e m e n t in habitat quality or transfers of organisms over long distances, as they seem to, a manager can attempt to increase rates of colonization by creating n e w habitats and restoring connectivity. This is vital. Many British butterflies are declining because the creation of n e w habitats has decreased rather than because ConservationBiology Volume8, No. 2,June 1994 Thomas local extinction rates from existing habitats have increased (Thomas. 1993). Mosaics and Metapopulations I argued that habitat dynamics rather than stochastic factors are the key to the persistence of m a n y real populations and metapopulations. Most extinctions are the result of deterministic population responses to a deterioration of conditions; m o s t observed colonizations follow an i m p r o v e m e n t in conditions near an existing local population or the transfer of organisms across some barrier to dispersal. Species track suitable environmental conditions, becoming locally extinct w h e r e conditions are no longer suitable for them and colonizing w h e r e conditions improve ( o v e r limited distances). Species persist in regions w h e r e they are able to track the environment, and they b e c o m e extinct if they fail to keep up with the shifting habitat mosaic. For many island species, the loss of suitable e n v i r o n m e n t conditions throughout their limited range has resulted in species extinction. The d e v e l o p m e n t of m e t a p o p u l a t i o n t h e o r y has played a crucial role in expanding our perspective on local to regional persistence, but existing models need to be superimposed on an environmental mosaic which in many cases will itself be spatially dynamic (see Southw o o d ' s [1977] habitat templet theory). This approach has advantages over existing metapopulation theory. Emphasis on the deterministic factors that cause species declines and population extinctions will focus attention on those factors that must be manipulated if a decline is to be checked. Emphasis on changes in the environment that p r e c e d e colonization will focus attention on factors that could result in species recovery. Can n e w m a n a g e m e n t a p p r o a c h e s create suitable habitat within colonization distance? If not, can sufficiently large areas of suitable habitat be created elsew h e r e that would support separate, viable populations, or can networks of habitat be created and p r o t e c t e d elsewhere that would support n e w viable metapopulations following introduction? The environmental mosaic approach also shifts the emphasis away from discrete patches. Population declines in large patches may b e as worrying as local extinctions in small patches, and expansion of patches may be as valuable as colonization of small additional patches. Decreases and increases in patch areas may be as amenable to m a n a g e m e n t as losses and gains of whole patches. Patch enlargement and i m p r o v e m e n t of the quality of existing patches are important conservation options. An environment mosaic perspective shifts the emphasis onto transient dynamics and away from the equilibrium (balance) concept of metapopulation dynamics, Thomas for w h i c h there is little e v i d e n c e in nature (Harrison 1994). Rates o f e x t i n c t i o n and colonization are important to persistence, b u t t h e y can b e in balance only w h e n the e n v i r o n m e n t is static o r w h e n the loss and creation o f suitable e n v i r o n m e n t a l conditions are themselves in balance. If m o s t major c h a n g e s in the distribution o f relatively sedentary species are driven b y changes in the spatial distribution o f suitable habitats, as I believe, conservation m u s t focus o n maintaining habitat continuity. For species o c c u p y i n g persistent habitats, the emphasis is o n habitat preservation. For species o c c u p y i n g shortlived or d y n a m i c habitats, the emphasis is o n ( 1 ) preservation and m a n a g e m e n t o f existing habitats, ( 2 ) preservation of sufficiently large areas or connected n e t w o r k s o f reserves that natural d y n a m i c s can be relied o n to p r o d u c e n e w habitats, and ( 3 ) creation of n e w habitats w i t h i n colonization distance. Acknowledgements F~¢iromne~tal T ~ g by Rare Species 377 Harrison, S. 1994. Metapopulations and conservation. Symposium of the British Ecological Society in press. Hochberg, M. E., J. A. Thomas, and G. W. Elmes. 1992. A modelling study of the population dynamics of a large blue butterfly, Maculinea rebelg a parasite of red ant nests. Journal of Animal Ecology 61:397-409. Jordano, D., E.C. Retamosa, and J. Femfindez Haeger. 1991. Factors facilitating the continued presence of Colotis evagore (Klug, 1829) in southern Spain. Journal of Biogeography 18:637-646. Kindvall, O., and I. Ahl6n. 1992. 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