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Multimodal niche-distribution, metapopulation theory and adaptation to stressful environments: Should they be included in models of range-contraction? E. VIRGÓS Escuela Superior de Ciencias Experimentales y Tecnología. Dpto. Matemáticas, Física Aplicada y Ciencias de la Naturaleza. Área de Biodiversidad y Conservación. C./Tulipán. s/n. 28933. Móstoles (Madrid). España. E-mail: [email protected]

Introduction Modern biogeography has largely been devoted to ascertaining how factors linked to geographical, evolutionary and ecological processes affect species-distribution and the speciation and extinction rates of different taxa (Myers and Giller, 1988; Lomolino and Brown 1998). In addition, the knowledge of how species interact with environmental perturbations is of vital interest in the conservation of biodiversity (Raup1991, Caughley, 1994; Channell and Lomolino, 2000a; b). Regarding this point, the nature of range-contraction in species is a key element in understanding the forces that cause extinction (Simberloff, 1986; Caughley, 1994; Lomolino and Channell, 1998; Channell and Lomolino, 2000 b). Two alternative and mutually exclusive hypotheses have been proposed to explain patterns of range-contraction in species: the demographic hypothesis and the contagion hypothesis (Lomolino and Channell, 1995; Channell and Lomolino, 2000a; b). The first is based on distribution models rooted in the niche concept (Brown, 1984; Brown, 1995) and on the small-population paradigm for species conservation (Caughley, 1994). The second is based on the declining-species paradigm (Caughley, 1994; Channell and Lomolino, 2000b). The demographic hypothesis is an extension of Brown’s niche hypothesis and other related issues (Hengeveld and Haeck, 1982; Brown, 1984, 1995; Brown et al., 1996). The niche ISSN: 1695-6370

hypothesis indicates that the density and performance of individuals decreases from central to peripheral populations as a consequence of a concomitant impoverishment of the spatially correlated resources that constitute the species-niche (Brown, 1984; Brown and Maurer, 1989; Brown, 1995). Based on these ideas, the small-population paradigm predicts that peripheral populations will be more prone to extinction than central ones due to low population density and higher temporal variability in density (Richter-Dyn and Goel, 1974; Pimm et al., 1988; Tracy and George, 1992; Caughley, 1994). This hypothesis has been assumed as fact, and most conservation practices have been guided by its ideas. However, several recent papers, especially Channell and Lomolino (2000a; b), indicate that peripheral populations show higher persistence than central ones, a fact that challenges old hypotheses and perceptions concerning this question. These authors suggest that the contagion hypothesis explains observed patterns better than the demographic hypothesis. The contagion hypothesis posits that the geographical dynamics of extinction factors play a key role in shaping the rangecontraction of species. In particular, it is suggested that historical and recent trends in the spread of human disturbance could be the main factor responsible for shaping the nature and dynamics of range-contraction. The data from a diverse group of organisms indicates that this pattern is very plausible Acta Granatense, 4/5: 71-76, 2006

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and Channell and Lomolino (2000a; b) propose a new paradigm for species conservation-peripheral populations may be more resistant to extinction as a consequence of a pure diffusion model which does not take demographic and niche constraints into account. Nevertheless, both proposed alternatives may be valid and, in this paper, I suggest that the demographic hypothesis may explain some anomalous cases and may interact with the contagion hypothesis as an underlying mechanism that explains patterns of range-contraction. My suggestion is based on some probably inadequate assumptions regarding the contagion hypothesis per se, as well as on a broader and more realistic view of the demographic hypothesis and the adaptive response of individuals living at the edge. Are the assumptions contained in the contagion hypothesis regarding the spread of disturbance realistic? The contagion hypothesis considers that perturbations begin on one side of the edge of the species’ distribution and then spreads passively and homogeneously across the space. This is certainly true in some cases, although perturbations probably have a more opportunistic and random nature, and they may begin either at the edge or in the centre of populations. In addition, the spreading process is not necessarily homogeneous; rather, perturbations possibly originate at different points and progress in different directions. The influence of the perturbation on each new area reached is very dependent on environmental and population (e.g. demographic) features, and it is predictable that even nearby areas may be influenced in very different ways by these particular features which may produce different speeds and directions of disturbance-spread. All these points suggest that there may be other alternative and plausible processes

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underlying mechanisms of range contraction, although the final result may be a higher resistance within peripheral populations. Unimodal vs multimodal niche-models in demographic hypothesis Other potential drawbacks of the original test of contagion hypothesis described by Channell and Lomolino (2000a; b) are related to its view of the nichedemographic hypothesis. Although the niche hypothesis originally formulated by Brown (1984) indicates that the density and performance of individuals decreases from core to peripheral populations, new models and data suggest that the pattern is not general and shows numerous and important exceptions. Lawton (1993) and several workers from Brown’s group (Brown, 1995; Brown et al., 1996) have indicated over the last few years that the pattern may not be as lineal as had initially been proposed; instead, there are a texture of the abundance composed by several peaks of high abundance and individual performance, as well as valleys of low abundance and individual performance (‘multimodal pattern’ Lawton, 1993; Brown et al., 1996). These multimodal patterns are as likely to be found in the middle of the geographical area as in peripheral locations. Thus, some marginal geographical populations could reach high density with well-suited individuals because they live in ‘ecological cores’, areas with high habitat suitability for the species (Carter and Prince, 1985; Caughley et al., 1987; Virgós and Casanovas, 1999). In contrast, some central areas could show very low population density, including the complete absence of the species (gaps) due to the lack of adequate habitats given the effects of competitors, predators or climate (Jeffries and Lawton, 1984; Lawton and Woodroffe, 1991, own unpubl. data) and the lack of an adequate adaptive response to new environmental factors. Therefore, the species would live in the so-called ‘ecological edges’ within the

ARTÍCULOS DE REVISIÓN middle of the distribution range (Brown et al., 1996). In a multimodal pattern of abundance, Lawton (1993) proposes that rangecontraction may follow a clearly different pattern from the unimodal distribution. In this case, it is predicted that populations retract and only persist in particular hotspots, areas where individuals show good performance and high fitness or are farther from sources of disturbance. The resulting pattern of species persistence may, therefore, not be as simple as in the unimodal pattern and may be very taxa or location-specific. Moreover, multimodal patterns may be refined by the new theories of metapopulation applied to species distribution (Lennon et al., 1997). Dynamics in peripheral and central populations may be very different and the result of many different factors (Parsons, 1991; Lawton, 1993). In central areas, habitat suitability and niche requirements may be more determinant of species abundance (Andrén, 1994; Lennon et al., 1997), and extinction patterns may be an epiphenomenon of the distribution of abundances and resources within the space. If the species presents a largely multimodal pattern with low connectivity, sub-populations may be treated in a very similar way to isolated populations at the edge. On the other hand, if the species is distributed in a continuous way, simple diffusion models may feasibly explain patterns of contraction. Peripheral or isolated populations in central areas show the same fragmented patterns. In this situation, expansions and contractions may be more dictated by the degree of isolation or area features than by niche requirements (Carter and Prince, 1981; Lennon et al., 1997). However, in these populations, random diffusion may be prevented by the isolation of sub-populations that, ultimately, may conform a metapopulation system with independent demographic dynamics (Hanski, 1991; Harrison, 1994). Metapopulation theory predicts that, paradoxically, isolation

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may enhance the survival of sub-populations because it avoids the spread of risks (e.g. disturbances, den Boer 1981, Harrison and Quinn, 1989). In the periphery and the hotspots of central areas, it is predictable that populations may be more resistant to extinction, a result consistent with the findings of Channell and Lomolino (2000a; b) although this situation may be caused by these different processes. New support for multimodal patterns of abundances: the role of genetic diversity and available metabolic energy in adaptation at the edge Multimodal patterns of abundance have received additional strong support from studies of organisms living under stress (Hoffmann and Parsons, 1991). These studies show that individual living at the edge present, on average, higher resilience and higher adaptive performance than those individuals living in more central or apparently adequate areas. Peripheral populations are normally composed of individuals that in some cases need to cope with more severe and harmful environmental conditions, normally at the extremes of the species’ habitat tolerance (Hoffman and Blows, 1994). In these situations, strong directional selective pressure may induce the survival of those genotypes that are able to cope with this particular selective regime (García-Ramos and Kirkpatrick, 1997, Kirkpatrick and Barton, 1997). This process may induce a rapid change in those traits that are key to survival or reproduction and thereby produce individuals that are locally highly adapted (Boag and Grant, 1981), with a fitness that differs little from or is even higher than central populations (see Carter and Prince, 1985; Hoffmann and Parsons, 1991; Hoffmann and Blows, 1994). This process has been largely hypothesised as the most relevant for explaining expansions in the fundamental niches of some species (Holt and Gaines, 1992; Kawecki, 1995; Holt and Gomulkiewicz, 1997). However, it has been challenged by some models and

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theoretical suggestions that have pointed out the lack of generality of this process due to a combination of low heritability of the key traits (as a consequence of directional selection), low genetic variance in marginal populations (although other new evidence indicates that populations under stress show large genetic variances, Parsons 1991) and the negative influence of migration from central populations which may interrupt the co-adapted genetic background of peripheral populations (Mayr, 1963; Hoffman and Blows, 1994; Kirkpatrick and Barton, 1997). All these concerns may be counterbalanced by several potential mechanisms such as the high spatial interruption of populations (dispersal may be very rare), high selective pressures from key traits in relation to immigration rates, genotype-environmental interactions causing negative selection of ‘core’ genes in the new environment and other genetic processes (Hoffman and Blows, 1994; Kirkpatrick and Barton, 1997). However, if some of these mechanisms are present, peripheral populations may be formed of highly adapted individuals, probably with high fitness and performance. Thus, these populations are probably not more prone to extinction than central ones. This result should be consistent with the multimodal pattern of species abundance, which indicates that some (or most) peripheral areas may be good for populations, while some central populations may be mis-adapted. This may explain why, in general, peripheral and central populations are equally adapted. Nevertheless, this then begs the question why peripheral populations are more resistant than central ones. The answer comes from studies into the adaptation of individuals to stressful environments. In these situations, the fitness of individuals may be dictated by the relationship between genetic variability and the metabolic energy available to cope with environmental challenges, which may differ between peripheral and central populations (Hoffman and Parsons, 1991; Parsons 1991).

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Species tend to disappear when the metabolic energy available to individuals or their low genetic variability is not enough to cope with stress, a situation that may be a deterministic process underlying the appearance of edges in the distribution of species. Some evidence indicates that in peripheral but usually occupied areas, as a consequence of the recurrent higher stress levels, populations may exhibit high genetic variability (Parsons, 1991) which may favour rapid phenotypic changes whilst at the same time retaining enough available metabolic energy to accommodate adaptive change. In contrast, populations of more central regions may lack sufficient genetic variability to cope with stress, even if they have high available levels of metabolic energy (Parsons, 1991). In addition, some data has pointed out that populations that are under stress may deal better with new stress than others in more benign conditions (e.g. core populations, Hoffman and Parsons, 1991). In this situation it can be predicted that some perturbation (e.g. human) may possibly be more harmful to persistence in these latter populations than in those more adapted to stressful situations. In this case, range contraction could proceed in a similar way to that in the observed pattern, with a larger number of populations persisting at the border where the populations are stressresistant than in central areas where species are not so well-adapted to stressful conditions. Epitome All these above-mentioned facts complicate the simple interpretation of range-contraction as a random diffusion of disturbances across a space. The contagion hypothesis is a challenging and seminal proposal because it shows that the older conceptions are wrong, and proposes a search for new mechanisms and interpretations of patterns. However, it needs more complex and realistic

ARTÍCULOS DE REVISIÓN assumptions and theoretical background in order to delve into the processes shaping extinction patterns and which may determine conservation priorities and guidelines. I suggest that new tests are needed which take into account different patterns of hot-spot distribution and perturbation features (initial position and number of initial points) and how they affect the centrality index proposed by Channell and Lomolino (2000a; b) over time. Simulation models that consider these realistic complexities may be compared to actual data in order to evaluate the relative performance of the different proposed mechanisms. These tests may help to gain more generality in explaining extinction patterns and additionally may account for taxa-specific or region-specific anomalies in data.

Agradecimientos. S. Cabezas-Díaz and J. G. Casanovas read and improved earlier drafts of this manuscript. M. Lockwood helps me with the english.

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