<<

Kelly Marie Henry NRS 534 – of Fragmented Landscapes May 18, 2005

Habitat fragmentation: the theories which provide the framework for the study of fragmentation

The common occurrence of results not only in habitat loss and habitat degradation, but also in fragmentation of the remaining habitat. A focal point for the research of many landscape ecologists is on the effects of to the individuals, , and experiencing this phenomenon. Habitat fragmentation can be defined as a process resulting in the transformation of a large section of relatively homogeneous habitat into smaller habitat patches of a heterogeneous composition (Fahrig 2003; Reed et al. 1995). Of particular importance is that the resulting smaller are typically isolated from each other by a matrix of habitats unlike the original. The concepts many landscape ecologists use when formulating habitat fragmentation hypotheses are not new ideas to the discipline of ecology. Two of the main theories providing the backbone to habitat fragmentation studies, the island theory and the theory, were originally developed to explain observations made in and ecology (Collinge 1996). Some common parameters examined when studying habitat fragmentation include the size, the degree of isolation, the context (matrix), and the degree of heterogeneity of the fragment as well as the impact of edge on the fragment. Island Biogeography Theory The island biogeography theory, originally proposed by MacArthur and Wilson in 1967, states that the size of an oceanic island and its distance from a mainland source of colonizing influences the number of species present on that island. While it is evident that the island biogeography theory was originally developed to explain species composition on oceanic islands, landscape ecologists studying habitat fragmentation apply the theory to the terrestrial islands created by habitat fragmentation (Fahrig 2003; Whittaker 1998; Collinge 1996). Habitat fragmentation research structured around the island biogeography theory typically focuses on the size of the fragment and the degree of isolation of the fragment.

1 The theory of island biogeography formed the basis of a study conducted by Walters et al. (1999) who examined the adverse effects of habitat fragmentation on brown treecreepers (Climacteris picumnus). Upon completing their research, Walters et al. (1999) found evidence that brown treecreepers experience lower male to female pairing success due to disrupted dispersal patterns in fragmented habitats versus unfragmented habitats. Another study with framework centered around the island biogeography theory was that of Davies and Margules (1998) who studied populations of carabid beetles. Based on previous studies, these scientists hypothesized that carabid beetle would decrease in fragmented habitats, and carabid beetle would decrease with the occurrence of fragmentation, with decreasing size of the fragment and with proximity to the edge of the fragment. Upon completing the study, Davies and Margules found that habitat fragmentation did, in fact, impact carabid beetle species richness and it appeared to alter species composition as well. Furthermore, habitat fragmentation did appear to decrease the abundance of the two species experiencing complete isolation due to habitat fragmentation (the other six species examined were not completely isolated). Metapopulation Theory The second theory supporting habitat fragmentation research is the metapopulation theory. Collinge (1996) defines a metapopulation as “a set of spatially separated groups of conspecific individuals.” Originally developed by Levins (1969) in the late 1960’s, the metapopulation theory states that while local populations of experience periods of colonization and events, the metapopulation as a whole continues to thrive. In order to be considered a metapopulation, the subpopulations must remain interconnected by , extinction, and recolonization (Whittaker 1998). There are two types of metapopulation models, the classic model and the source-sink model. The classic model assumes all subpopulations are of the same size, while the source-sink model assumes a large core population that persists indefinitely during the periods of extinction and recolonization experienced by the smaller sink populations. Habitat fragmentation research incorporating the metapopulation theory typically focuses on the connectivity and the exchange of individuals between habitat fragments. The metapopulation theory was applied in a study by Dunham et al. (2003) examining the short and long-term impacts of on native fish populations. The study found that the persistence of local native fish populations in larger habitat patches could

2 be explained by the larger able to inhabit the patch or by the increased habitat heterogeneity frequently existing in these larger habitat patches. However, the persistence of populations in smaller habitat patches was likely due to the dispersal of individuals from nearby populations. It is the combination of both the island biogeography theory and the metapopulation theory, which together support habitat fragmentation studies. Although the island biogeography theory focuses on the size and degree of isolation of habitat fragments and the metapopulation theory focuses on connectivity and exchange between habitat fragments, many researchers study different combinations of these effects on individuals, populations, and ecosystems. Both theories have a strong spatial component, which causes the two theories to become tightly interwoven in studies of habitat fragmentation. A strong emphasis is placed when studying habitat islands on the degree of isolation or the connectivity of the habitat with surrounding patches. The spatial location of individuals, populations, and communities influences the metapopulation dynamic. Hanski (1998) states that the spatial structure of the metapopulation is as important in determining the metapopulation dynamic as birth and death rates since the spatial structure allows for immigration. Following an event of habitat destruction resulting in habitat fragmentation, a patch typically experiences faunal relaxation (Viveiros de Castro and Fernandez 2004; Whittaker 1998). Once fragmentation occurs, the newly created patch is supersaturated with species. After the “” or time lag following the fragmentation is over, the number of species slowly decreases until a new equilibrium level is achieved (Hanski 1998). However, immigration and extinction both continue to occur during the relaxation process and after equilibrium has been established. In general, the response to fragmentation by a metapopulation is non-linear due to the manner in which habitat connectivity is lost (Hanski 1998). However, evidence does suggest that relaxation and the sequence of species lost are highly structured and should be predictable (Viveiros de Castro and Fernandez 2004). The idea of a metapopulation allows for satellite populations to come and go, with the core population remaining indefinitely. However, due to the stochastic of faunal relaxation, species can become extinct throughout entire . Common parameters used in habitat fragmentation studies When studying the effects of habitat fragmentation on an , landscape ecologists focus on a wide variety of habitat parameters. Some recurring themes in the

3 study of habitat fragmentation include the size, the degree of isolation, the context (matrix), and the degree of heterogeneity of the fragment, as well as the impact of edge on the fragment. The size of the fragment influences the ecological process able to occur within the fragment (Collinge 1996). As habitat fragments become more isolated, the dynamics within the fragment become increasingly important. It is therefore important to maintain a minimum dynamic area, defined by Pickett and Thompson in 1978 as the “smallest area with a natural regime, which maintains internal recolonization sources, and hence minimizes extinction” (Dunham et al. 2003). Many studies have found a positive correlation of decreasing species richness and individual abundance with decreasing fragment size due to low and survival rates in the smaller fragments (Smith and Hellmann 2002; Collinge 1996). It should be noted that not all studies examining the size of a fragment relative to its impact on a population find negative effects associated with decreasing patch size (Eggleston et al. 1999; Davies and Margules 1998). The degree of connectivity and the composition of the surrounding matrix influence the species interactions between habitat fragments. The persistence of a population in the face of increasing habitat fragmentation can be explained by the metapopulation theory only if some degree of connectivity is maintained between the fragments. As connectivity decreases, population persistence decreases due to isolation from the supporting metapopulation (Dunham et al. 2003). The context of surrounding habitat will influence the degree and type of interaction between the fragment and the surrounding area. The degree of dissimilarity strongly influences the flow of nutrients and materials, as well as the persistence of plant and species between the fragment and the surrounding matrix (Mesquita et al. 1999; Collinge 1995). When the components of the matrix are structurally similar to the components of the fragment, the impacts of fragmentation are less as species in the fragment are able to use areas outside of their fragment for habitat or interfragment movement (Viveiros de Castro and Fernandez 2004). Degree of heterogeneity and quantity of edge habitat both influence the diversity, abundance, and composition of species within a fragment. Studies suggest that the more heterogeneous a fragment the greater number and variety of species the fragment will support. The mosaic of a habitat fragment may directly or indirectly impact , abundance, or behavior (Eggleston et al. 1999; Whittaker 1998). An important occurrence associated with the fragmentation of a habitat is the increase in the

4 length of the boarder between the habitat fragment and surrounding habitat. Increasing the edge along an area leads to increases in , , and wind, and decreases in relative humidity (Whittaker 1998; Collinge 1996). These changes in microclimate impact the plant and animal communities at the edge of the habitat fragment. In particular, edges usually contain more (Collinge 1996). Landscape ecologists have developed the parameters discussed above as well as others for measuring the impacts of habitat fragmentation on individuals, populations, and ecosystems. In addition, their studies are based on two well researched theories of community and . However, throughout habitat fragmentation literature there is a thread of disbelief that the study of habitat fragmentation is different from the study of habitat loss. Many authors emphasize the difficulty in separating the negative effects of habitat loss from the positive and negative effects of habitat fragmentation (Fahrig 2003; Walters et al. 1999). This has proven a trying task to many landscape ecologists, and brings up the question, “is fragmentation a useful term?” (Fahrig 2003).

5 Annotated Bibliography:

Collinge, S.K. 1996. Ecological consequences of habitat fragmentation: implications for landscape architecture and planning. Landscape and Urban Planning. 36:59-77.

This review addresses the importance of studying the impacts of habitat fragmentation on the ecology of various systems. While the fragmentation of landscapes resulting in transformation, habitat loss, and patch isolation can occur naturally, it appears are increasing the rate of land conversion and subsequent habitat fragmentation. Collinge provides an overview of two theories behind the study of habitat fragmentation, the island biogeography theory and the metapopulation theory. The island biogeography theory examines the influence of habitat fragment size and degree of isolation on the composition of species within the fragment. The metapopulation theory uses the concept of a metapopulation (“a set of spatially separated groups of conspecific individuals”) to describe the and subsequent recolonization of species in patchy or fragmented habitats. While neither of these theories were developed directly to explain the impacts of habitat fragmentation, they have been applied to the development of experimental hypotheses and designs studying the impacts of habitat fragmentation. Collinge then reviews existing literature summarizing the various aspects of habitat fragmentation including the size, connectivity, shape, context, and heterogeneity of the fragment as well as the effect of edge on the fragment. In conclusion, the importance of maintaining fragment connectivity and heterogeneity as well as decreasing the amount of edge is emphasized in order to mitigate the negative impacts of habitat fragmentation. This review article provided a comprehensive explanation of habitat fragmentation, the theories supporting habitat fragmentation studies, and the parameters used to examine the effects of habitat fragmentation.

Coulson, R.N., B.A. McFadden, P.E. Pulley, C.N. Lovelady, J.W. Fitzgerald, and S.B. Jack. 1999. Heterogeneity of forest landscapes and the distribution and abundance of the southern pine beetle. and Management. 114:471-485.

Coulson et al. analyzed how the southern pine beetle, Dendroctonus frontalis, perceives and responds to habitat heterogeneity. In light of activities altering both the content and the context of the habitat of the southern pine beetle (as well as the habitat of other organisms), it is necessary to determine if these activities are enhancing or inhibiting the beetle’s habitat. By creating a functional heterogeneity map, Coulson et al. were able to analyze how the arrangement of landscape elements influenced the distribution and abundance of the southern pine beetle. Acceptable tree species, the susceptibility of forest stands, and lightening-struck trees are all important elements of the landscape essential to the persistence of metapopulations of southern pine beetles. Using the angular moment of inertia index, functional heterogeneity, and connectivity of southern pine beetle habitat were quantitatively measured and then mapped. This article was not particularly useful for explaining the theories behind habitat fragmentation, however, it did provide a good example of a method for assessing how habitat fragmentation effects the distribution and abundance of the southern pine beetle.

Davies, K.F. and Margules C.R. 1998. Effects of habitat fragmentation on carabid beetles: experimental evidence. Journal of Animal Ecology. 67:460-471.

6 This study examines the effects of habitat fragmentation on the carabid beetle species richness and abundance in fragmented forest habitats relative to non fragmented forest habitats. Based on previous studies, Davies and Margules hypothesized that carabid beetle species richness would decrease in fragmented habitats, and carabid beetle abundance would decrease with the occurrence of fragmentation, with decreasing size of the fragment, and with proximity to the edge of the fragment. The experiment was conducted in south-eastern Australia using three experimental fragment sizes each replicated six times. Four of the experimental eucalyptus forest plots were surrounded by pine forest, while the other 2 experimental eucalyptus forest plots were retained within a surrounding eucalyptus forest matrix. Poisson and logistic regressions were used to analyze the data as the resulting experimental data was asymmetrical versus normally distributed. Upon completing the study, Davies and Margules found that habitat fragmentation did impact carabid beetle species richness, although it did appear to alter species composition. Habitat fragmentation did appear to decrease the abundance of the two the two species experiencing complete isolation due to habitat fragmentation (the other 6 species examined were not completely isolated). No clear trend in carabid beetle abundance was found relative to habitat size or proximity to edge of fragment. Davies and Margules provide a classic example of a study examining the effects of habitat fragmentation on a particular species incorporating ideas from both the island biogeography theory as well as the metapopulation theory.

Dunham, J.B., M.K. Young, R.E. Gresswell, and B.E. Rieman. 2003. Effects of fire on fish populations: landscape perspectives on persistence of native fishes and nonnative fish invasions. Forest Ecology and Management. 178:183-196.

In this article, fire is identified as an agent of disturbance, and Dunham et al. explore short and long-term impacts of fire on native fish populations in order to aid in the development of a successful fire management technique. Fire is recognized as a natural disturbance that may be necessary to the persistence of many native fish populations. However, fire may decrease the connectivity of a landscape, and subsequently decrease the persistence of a population by causing isolation from the metapopulation. Dunham et al. review a study by Detenbeck et al. (1992), which examined the impacts of fish populations to “pulse” (short-term) versus “press” disturbances (long-term). Detenbeck et al. found that recovery was dependent upon the length of the disturbance and the location of the populations from the source population as well as specific lifecycle requirements for the population at hand. In conclusion, several fire management approaches are addressed by Dunham et al. including pre-fire management of the system, managing the fire once it has begun, managing the system after the fire, and monitoring for adaptive management. The importance of maintaining connectivity throughout a metapopulation is strongly emphasized throughout this article, which provides an excellent example of the metapopulation theory applied to fragmented habitats.

7 Eggleston, D.B., W.E. Elis, L.L. Etherington, C.P. Dahlgren, and M.H. Posey. 1999. responses to habitat fragmentation and diversity: Habitat colonization by estuarine macrofauna. Journal of Experimental Marine and Ecology. 236:107-132.

Eggleston et al. studied the interactive impacts of patch size, habitat diversity, and experimental site on the colonization of benthic marine macrofauna. They tested their hypotheses by placing trays filled with either, , shell, or a mixture in a subtidal located in within Back Sound, NC. Previous studies have determined that the mosaics of habitat types may directly or indirectly impact predator distribution, abundance, and behavior. In addition, the special arrangement of habitat fragments may also impact water flow which is responsible for the distribution, settlement, and accumulation of drift or as well as animal behavior. Before beginning the study, Eggleston et al. predicted colonization would be greater in smaller patches as the probability of encounter with the patch would be increased. Also, they predicted that smaller macrofauna would show a stronger response to habitat patchiness than large organisms, and that colonization would be higher in mixed habitat plots versus monotypic plots. They found that organism response to the spatial arrangement of habitats was dependent upon the spatial scale, the habitat type, and the organism’s body size. The study showed one very important implication for management; experiences greater negative impacts with the fragmentation of oyster shell habitats than with the fragmentation of either seagrass or a mixture of both habitats. Unfortunately, many of the western Atlantic subtidal oyster habitats have been severely fragmented.

Fahrig, L. 2003. Effects of habitat fragmentation on biodiversity. The Annual Review of Ecology, , and . 34:487-515.

In this review article, Fahrig identifies many of the inconsistencies in habitat fragmentation studies. While there is no shortage of literature exploring the effects of habitat fragmentation on ecosystem biodiversity, the results of all these studies can be difficult to interpret. Authors tend to measure habitat fragmentation using different experimental designs, which has leads to varying conclusions in regard to the impacts of habitat fragmentation on biodiversity. Habitat fragmentation can be measured as a process or as a pattern. When measuring habitat fragmentation as a process, the study will typically only examine one continuous landscape and one fragmented landscape causing the results to be largely comparative and qualitative. When measuring habitat fragmentation as a process, the scientist can quantitatively measure the effects of (a) habitat loss, (b) change in habitat configuration, (c) decrease in patch size, or (d) increase in patch isolation. Which variable(s) measured in the study, can influence the conclusions the scientist draw. While the effects of habitat loss are frequently negative, the effects of habitat fragmentation can be both positive and negative. Negative effects of habitat fragmentation result from patches that are too small to support a population as well as from negative . The positive effects of habitat fragmentation result from (1) higher immigration rates when there are many small patches close together. In addition, (2) when the amount of habitat is held constant as the degree of fragmentation increases, then the dispersal distance between patches will decrease. Furthermore, (3) increasing fragmentation, increases land complementation, resulting in increased biodiversity. Increasing fragmentation has positive effects for (4) species which require more than one habitat, and (5) the effects of edge may be positive for some species. Fahrig emphasizes the importance of determining the effects of habitat fragmentation on

8 biodiversity, separate from the effects of habitat loss on biodiversity. This review is a must read for anyone studying habitat fragmentation. Throughout the article, Fahrig brings up numerous controversial points causing the reader to questions whether the study of habitat fragmentation measures effects separate from those of habitat loss. By the end of the article it is impossible not to ask the question, “Is fragmentation a useful term?”

Hanski, I. 1998. Metapopulation Dynamics. Nature. 396:41-49.

In this review article, Hanski emphasizes the importance of studying the spatial structure of populations. It is the spatial location of individuals, populations, and communities, which influence the metapopulation dynamic. Hanski believes the spatial structure amongst populations is as important as the birth and death of individuals within populations when determining local extinction. Throughout the review, Hanski addresses aspects of , metapopulation ecology, and , focusing on the theory of metapopulation ecology. Extinction-colonization and regional stochasticies and their influence on the spatial structure and persistence of metapopulations are discussed. Of particular interest was Hanski’s description of the response of metapopulations to habitat destruction. Metapopulations respond to habitat destruction and the subsequent loss, decrease in quality, and fragmentation of the habitat (1) in a non linear manner, (2) with a time lag or “extinction debt.” The third conclusion in regards to the response of metapopulations to habitat destruction is the number of empty habitats before the destruction equals the extinction threshold of the metapopulation, this is also known as “Levin’s Rule.” In conclusion, is useful because it allows for complex spatial patterns in seemingly uniform environments, and it allows for species to be absent where conditions are favorable and for species to be present in locations where the environment is unfavorable. As a final caution, Hanski warns ecologists and conservationist not to assume all species exist as metapopulations.

Smith, J.N.M. and J.J. Hellmann. 2002. Population persistence in fragmented landscapes. Trends in Ecology and Evolution. 17:(9)397-399.

Smith and Hellmann review a study by Lesley and Michael Brooker examining the impact of habitat fragmentation on the reproduction, survivorship, and movement of the blue-breasted fairy-wren, Malurus pulcherrimus. While many conservation biologists believe dividing habitats decreases habitat area, which intern decreases reproduction as well as survival, many studies of habitat fragmentation do not exhibit these results. Smith and Hellmann review what they believe is one of the few studies demonstrative the negative effects of habitat fragmentation on a specific population. After carefully studying M. pulcherrimus populations in western Australia for five years, the Brookers found evidence of similar demographic behavior throughout different size habitat fragments. Wren reproduction was higher in smaller habitats, but wren survival was lower in these smaller fragments. Conversely, the reproductive success of wrens was poor in larger fragments due to brood . This study also demonstrated that poor habitat connectivity can leads to greater dispersal loss and a subsequent decrease in population.

Van Dyck, H. and E. Matthysen. 1999. Habitat fragmentation and insect flight: a changing ‘design’ in a changing landscape? Trends in Ecology and Evolution.

9 14:(5)172-174.

Van Dyck and Matthysen review a study conducted by Jane Hill, Chris Thomas, and Owen Lewis examining the impact of habitat fragmentation on the flight morphology of insects. Previous studies have shown that while in the presence of habitat fragmentation different species of insects do not experience the same morphological evolution with increasing isolation, many species of insects do show some type of morphological evolution. Evidence demonstrates that butterflies exhibit evolutionary response in flight morphology to changes in landscape structure. Hill et al. examined the butterfly, Hesperia comma, and found the thoraxes of individuals in metapopulations where habitat patches were further apart to be heavier than those of individuals in metapopulations where habitat patches were closer together. (The thorax of a butterfly contains the flight muscles.) Van Dyck and Matthysen also explore other explanations for changes in insect morphology with habitat fragmentation including changes in behavior with increasing isolation due to decreased population size within fragments. In addition, morphological evolution may occur with the change in habitat microclimate associated with habitat fragmentation. The changes in morphology associated with habitat fragmentation may not always favor increased mobility. While there are many implications for managing populations with short generations times and rapid evolutionary responses, one of the major threats for managing insect populations were evolution may favor a decrease in mobility is the threat of localized . The structure of this article is not particularly well organized, however the authors do bring an important point. All species do not react to the effects of increased isolation in the same manner. This is an important concept to keep in mind when studying the effects of habitat fragmentation on different species.

Viveiros de Castro, E.B. and F.A.S. Fernandez. 2004. Determinants of differential extinction vulnerabilities of small mammals in Atlantic forest fragments in Brazil. Biological Conservation. 119:73-80.

The authors initially identified that different species should have varying levels of vulnerability to fragmentation and that the ability to predict species vulnerability to fragmentation would be extremely beneficial to the management of fragmented . After fragmentation, forests experience a faunal relaxation, which leads to a decrease in species richness until a new levels of diversity able to be sustained by the current habitat fragments is achieved. After evaluating whether vulnerability could be predicted based on body size, , longevity or fecundity of the mammal, the pre-fragment population density of the mammal, or the surrounding matrix tolerance of the mammal, the authors found the only beneficial predictor of small mammals to habitat fragmentation was the mammal’s vulnerability to the surrounding matrix. The ability to live in the matrix and/or to travel through the matrix allows for a metapopulation to persist even after fragmentation. In conclusion, connectivity between forest fragments due to tolerance of the surrounding matrix allows for recolonization or immigration opportunities. This was another article which did not prove particularly useful for explaining the theories behind habitat fragmentation, however, it did provide a good example of the importance of the surrounding matrix in maintaining population persistence in the event of habitat fragmentation.

Walters, J.R., H.A. Ford, and C.B. Cooper. 1999. The ecological basis of sensitivity of brown treecreepers to habitat fragmentation: a preliminary assessment. Biological

10 Conservation. 90:13-20.

This study compared the demography and ecology of brown treecreeper, Climacteris picumnus, populations experiencing habitat fragmentation to those populations in unfragmented habitats. In order to asses the impacts of habitat fragmentation on the brown treecreeper, Walters et al. explored the possibilities of disrupted dispersal patterns, decreased fecundity due to , and decreased availability due to habitat degradation on populations experiencing fragmentation. Upon completing their research, Walters et al. found that it was not an increase in nest predation or a decrease in food quality that was causing the decline in the brown treecreeper populations with the increase in habitat fragmentation. Their evidence supported that in fragmented habitats brown treecreepers experience lower male/female pairing success due to disrupted dispersal patterns. Walters et al. believe the decrease in populations is due to the difficulty females experience when trying to locate vacant breeding habitats in the isolated fragments. The possibility also exists that if they do find a habitat, it may be rejected due to degraded conditions. Walters et al. provide another classic example of a study examining the effects of habitat fragmentation on a particular species incorporating ideas from the island biogeography theory.

Whittaker, R.J. 1998. Island theory and conservation. Island Biogeography: Ecology, Evolution, and Conservation. Oxford University Press, New York. 192-227.

In Chapter 9 of Whittaker’s book, he applies the island theory (developed by MacArthur and Wilson in 1967) to habitat islands within a fragmented landscape. Whittaker attributes the process of habitat fragmentation to the formation of habitat islands, however, he realizes that the separation between habitat islands and the subsequent movement of species may be “radically different” than between oceanic islands. In the chapter, several key concepts including minimum viable population size and minimum viable area are discussed. After introducing the concept of a metapopulation, Whittaker does an excellent job of incorporating both the island theory and the metapopulation theory when addressing conservation issues. A main emphasis in the study of habitat islands is on the degree of connectivity between different habitat patches. When applying the island theory to oceanic islands, the surrounding matrix is unimportant and it is assumed that the population of the island will eventually reach an equilibrium state. Conversely, when applying the island theory to habitat islands, it is important to remember the “flux of nature.” Physical and biological as well as episodic events will continue to act upon the habitat island. In addition, the connectivity with surrounding habitat patches will continue to act as a species filter. The combination of all these factors is likely to prevent a habitat island from ever reaching an equilibrium state. In conclusion, Whittaker cautions against oversimplifying island effects on fragmented habitat patches. For purposes of conservation, he recommends identifying the species most vulnerable to habitat fragmentation and working towards their preservation as the effects of connectivity versus isolation as well as the effects of increased amounts of edge are different for all species. This chapter provides an excellent overview of both the island biogeography theory (MacArthur and Wilson 1967) and the metapopulation theory (Levins 1969).

Additional References:

Levins, R. 1969. Some demographic and genetic consequences of environmental

11 heterogeneity for biological control. Bulletin of the Entomological Society of America. 15:237-240.

MacArthur R.H. and E.O. Wilson. 1967. The Theory of Island Biogeography. Princeton University Press. Princeton, NJ.

Mesquia, R.C.G., P. Delamônica, and W.F. Laurance. 1999. Effect of surrounding on edge-related tree mortality in Amazonian forest fragments. Biological Conservation. 91:129-134.

Reed, R.A., J. Johnson-Barnard, and W.L. Baker. 1996. Fragmentation of a forested Rocky Mountain landscape, 1950-1993. Biological Conservation. 75:267-277.

12