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Volume 2 † Number 2 † June 2009 10.1093/biohorizons/hzp017 ......................................................................................................................................................................................................................................... Research article Patterns of genetic diversity in populations of two bat species (Sturnira ludovici and Artibeus toltecus) in Cusuco National Park, Honduras Claire Asher* Department of Biology and Environmental Science, School of Life Sciences, University of Sussex, Falmer, Brighton, UK. * Corresponding author: 4 Villiers Walk, Newbury, Berkshire RG14 6SJ, UK. Tel: þ44 01635 821316. Email: claireasher13@googlemail.com Supervisors: Professor Adam Eyre-Walker, Department of Biology and Environmental Science, School of Life Sciences, University of Sussex, Falmer, Brighton BN1 9QG, UK and Dr Kimberley Hunter, Department of Biological Sciences, Salisbury University, Salisbury, Maryland 21801, USA. ........................................................................................................................................................................................................................................ Habitat loss, disturbance and fragmentation are thought to be major threats to many species, particularly those in habitats that are already rare. In this study, we examined whether habitat disturbance, primarily due to the cultivation of coffee, has had a major impact on populations of two species of bats in a Honduran cloud forest, using genetic diversity as a measure of population health. Bats were selected as the study species because they play a major role in seed dispersal within the tropics. I compared the genetic diver- sity of two frugivorous bat species, Sturnira ludovici and Artibeus toltecus, between two localities within Cusuco National Park; a buffer zone in which some human activity, including coffee plantations, is allowed, and the core zone in which no disturbance is permitted. Genetic diversity was assessed using intersimple sequence repeats, a technique similar to random amplification of polymorphic DNA (RAPD). I also measured various habitat variables including foliage height diversity (FHD), fruit availability, canopy cover, aspect of slope and angle of slope in the two sites. I found that FHD and fruit availability differed significantly between the two localities, with the buffer zone having higher values for both. Despite these differences in habitat, we found no significant differences in the level of genetic diversity between the two locations for either bat species. This may be because effective population sizes of the bats do not differ significantly between the sites, because of a lag between disturbance and population decline or because migration is sufficiently frequent to homogenize allele frequencies between the localities. Key words: genetic diversity, bat, cloud forest, conservation, habitat disturbance. ........................................................................................................................................................................................................................................ Honduras is the second largest country in Central Introduction America, and approximately half its land is covered by a Collectively, the Americas contain 916 million ha of tropical mosaic of pine-oak forest and montane forest. It is home forest, which is being destroyed faster than on any other con- to over 5500 vascular plants, of which 108 are listed as tinent, at a rate of 10 million ha a year. Of the 34 hotspots endangered. In addition to this, there are 410 known bird identified by Conservation International, 8 reside within the and mammal species, of which 26 appear on the IUCN Americas. Of these, the Mesoamerican hotspot is the red list. Despite this, it has been relatively overlooked in bio- largest, and the third largest in the world. diversity studies within Mesoamerica. All land higher than The Mesoamerican hotspot includes most of Central 1800 m has been designated as protected, and 25% of America and contains dry forest, lowland moist forest and the country’s forests lie within protected areas, covering a montane forest. It exhibits extremely high endemism of up total of 2.7 million ha. However, there has been little enfor- to 70% in the richest areas, where endemism is defined as cement of these areas and illegal logging is a severe problem. the percentage of species whose distribution is confined to Tropical forests can contain hundreds or even thousands that area, and may contain as much as 7% of the world’s of tree species, a significant proportion of which use animal- biodiversity. mediated seed dispersal. Between 50% and 90% of tropical ......................................................................................................................................................................................................................................... 2009 The Author(s). This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. 147 Research article Bioscience Horizons † Volume 2 † Number 2 † June 2009 ......................................................................................................................................................................................................................................... shrub and tree species are dependent on frugivorous ver- Although most studies have used species-richness and tebrates for seed dispersal. As well as distributing seeds abundance estimates to determine the affect of human dis- over a wide area, frugivores are important because the turbance on animal and plant populations, genetic methods passage of a seed through the digestive tract improves both can also be used to assess these questions. Species with seed viability and rapidity of germination. Compared with small, or declining, populations are likely to suffer from other frugivores, birds and bats have the greatest positive reduced genetic diversity due to inbreeding and genetic 7 15 effect on germination. However, bats are responsible for a drift. Inbreeding has been found to have deleterious greater amount of seed dispersal than birds, particularly effects on a variety of characteristics including sperm pro- in disturbed areas, where bats have been found to be the duction, female fecundity, juvenile and adult survival, and 10 15 primary seed dispersers. mating ability. Furthermore, reduced genetic diversity Bats are members of the order Chiroptera, one of the most may adversely affect the ability of a species to adapt to 11 15 diverse and widely distributed groups of animals. They are environmental changes. Small population size is therefore especially important in Neotropical forests, where they con- likely to further increase the chances of extinction. stitute 50% of all mammal species. Neotropical bats are Experimental evidence supports this, and a recent compari- members of the family Phylostomidae, of which there are son of genetic diversity in threatened and unthreatened 220 species, comprising 24% of the global total. species found that 77% of threatened species had lower The reliance of many tree species on frugivorous bats for genetic diversity, with an average reduction in heterozygosity seed dispersal has important implications for conservation of 35%. Conservation studies that ignore genetic factors and forest regeneration. Experimental exclusion of frugivor- are therefore likely to overestimate the probability of survival ous bats resulted in a 30% reduction in seed species rich- for threatened species. ness and research suggests that forest regeneration may This study uses intersimple sequence repeats (ISSRs), a already be being threatened by reduced seed dispersal. polymerase chain reaction (PCR)-based technique, to deter- Furthermore, it appears that there is a threshold bat popu- mine the level of polymorphism in populations of bats lation density, below which seed dispersal may cease living in pristine cloud forest, compared with those living 7 18 altogether. in a human-altered habitat. ISSR techniques involve ampli- Frugivorous bats have been found to be particularly toler- fication of nuclear DNA using a primer that targets the ant of human disturbance, perhaps because they have rela- repeating sequence of microsatellites. ISSR is identical to tively general habitat requirements. Some studies have RAPD, except that the primer sequence is based only on even found them to be more abundant in disturbed areas the repeating sequence, and therefore no information 14 19 because of the greater availability of fruiting plants. about flanking sequences is required to use the technique. However, they may rely upon pristine habitat for roosting ISSRs are therefore simpler and less expensive to use and sites, and studies on temperate bat species have found that may reveal a greater number of polymorphisms than 10 22 many species have very specific roosting preferences. If RAPD. ISSRs have been used in a variety of different 19, 22, 23 this is the case, then the loss of pristine forest may impair studies in plants, but have rarely been used in ver- the ability of frugivorous bats to aid regeneration in dis- tebrates before. turbed areas resulting in a vicious cycle of habitat degra- I have chosen two common species of frugivorous phyllos- dation. Thus, the effects of human activities on bat species tomid bat, Sturnira ludovici and Artibeus toltecus, to inves- need to be carefully monitored to prevent exacerbation of tigate this. A. toltecus has recently been reclassified into anthropogenic habitat change. the Dermanura genus, and in some of the literature, is now Bats may be considered keystone species, not only because referred to as Dermanura tolteca. For the purposes of this of their indispensable role in seed-dispersal, but also because paper, I will use the original, A. toltecus classification. of their involvement in a variety of ecological processes includ- These two species are among the most abundant species of 9 14 9 ing pollination and insect population regulation. Bats may Neotropical bat. A. toltecus is a canopy specialist, and also be useful as indicator species asthey are common and rela- fruit choice trials have indicated that A. toltecus preferen- 9 25 tively easy to capture. Furthermore, bat species richness and tially feeds on Constegia volcanalis. In contrast, diversity in Neotropical forests is positively correlated with S. ludovici is more generalist, feeding on a variety of fruits 9, 14 25 measures of vegetation structure. Bat species richness is from both canopy and ground-storey plants. However, highest in undisturbed forest, and the most abundant species about half of its diet is composed of fruits of Solanum 9 9 is characteristic of particular levels of disturbance. sp. which are found primarily in disturbed forest. Considering their abundance, and invaluable role in a I hypothesize that if habitat disturbance has had a major variety of ecosystem processes, understanding how impact on bat populations, then the genetic diversity Neotropical bats are affected by habitat disturbance is of S. ludovici and A. toltecus will be significantly lower in crucial to understanding how best to preserve the remaining the buffer zone than in the core zone of Cusuco National tropical forests. Park. ......................................................................................................................................................................................................................................... 148 Bioscience Horizons † Volume 2 † Number 2 † June 2009 Research article ......................................................................................................................................................................................................................................... For each bat, a 1 mm radius wing-punch was taken and Materials and Methods stored in ethanol in a 2.5 ml eppendorf tube. These were Study Site transferred back to the laboratory located at base camp. Wing-punches of S. ludovici and A. toltecus were then used Cusuco National Park (Fig. 1) is one of the smallest of the for genetic analysis. Five wing-punches were collected for country’s protected areas, located in the Paraiso valley each species at each site, producing a total of 20 wing-punch near San Pedro Sula, in the Northwest of the Country. samples for processing. It was established in 1959 and covers 23 440 ha of land. The park predominantly consists of cloud forest, Habitat Sampling a rare type of evergreen montane forest, which occurs only at sufficiently high altitudes, and in climate con- Habitat data were collected from two circular plots of 20 and ditions which cause regular contact between clouds and 40 m radius surrounding each mist-netting site. A total of 45 the vegetation. Cloud forest accounts for 2% of the samples were collected at each transect. Of these, 30 samples world’s tropical forest, but is known to exhibit exception- were collected within a 20 m radius, and a further 15 in a ally high endemism. Furthermore, cloud forests are 20–40 m radius. The latter points were then combined home to the wild relatives of many crop plants, including with 15 randomly selected samples from the 20 m radius, tomato, avocado, cucumber and potato. They are also to produce a total of 30 samples within the 40 m radius. essential in maintaining water supply to local people. The position of each sample point was determined using For example, 40% of the water supply to the capital, random numbers generated in Microsoft Excel. For each Tegucigalpa, is supplied by cloud forests in neighbouring point, a random number between 0 and 1 was generated national parks. and multiplied by 360 to produce a bearing from North. A Data were collected from two sites within Cusuco second random number between 0 and 1 was generated and National Park; Operation Wallacea Base Camp within the multiplied by 20 to produce a distance of up to 20 m. To core zone and a village called Buenos Aires in the buffer collect the samples from the 20 to 40 m radius, 20 m was zone. At each site, bats were captured using mist-nets setup added to the distance value. These two numbers together on transects surrounding the site. At each transect, six determined the position of the sample point with relation to 6m 2.5 m mist-nets with five shelves were set up the start point. This distance-based sampling method provides between the hours of 5 pm and 12 midnight. an easy way to determine and locate sample points, and the Figure 1. Map of Cusuco National Park. Source: Operation Wallacea (http://www.opwall.com). ......................................................................................................................................................................................................................................... 149 Research article Bioscience Horizons † Volume 2 † Number 2 † June 2009 ......................................................................................................................................................................................................................................... use of random numbers ensures that the points are selected in room temperature for 1 min. The column was then centri- an unbiased way and are well distributed across the study area. fuged at 8000 rpm for 1 min, and the elution process was The start point was selected in order to be as central as poss- repeated. The resulting purified DNA was then amplified ible within the area in which the mist-nets were located. Due using an ISSR PCR. This technique uses anonymous domi- to the structure of the terrain, some random points were not nant markers consisting of repeated sequences to amplify accessible because of barriers such as rivers and cliffs. When small sections of the DNA. a point arose that was not usable, it was skipped and the Following amplification, the DNA was run on a cambrex next point in the list was selected. flash gel (2.2%) to produce a visual representation of the In order to calculate the foliage height diversity (FHD), genetic constitution of each individual. ISSR primers consist a 3 m pole, marked into 1 m sections, was used. For each 1 m of short repeating sequences, which bind to complementary section, a cylinder of radius 1 m was imagined surrounding microsatellite sequences. Since ISSR primers do not include a the pole, and the number of branches intersecting the cylin- flanking region, no prior information about a species is der was noted. FHD was calculated as: required. A number of ISSR primers were available, and these had to be screened to find ones that successfully bind to the FHD ¼ log p e i DNA and show polymorphism between individuals. Initially, two samples from S. ludovici were amplified with each of three randomly chosen primers, and the resulting DNA was where p is the proportion of the total foliage counted which run on a flash gel. Two of these three primers showed poly- lies in the ith cylinder. morphism, both of which consisted of AG repeats. Based on The availability of fruit surrounding the sample point was this, a further three primers, also containing AG repeats were noted on a nominal scale of low to high. In addition to this, selected and used to amplify DNA from the same two individ- the angle of the steepest slope was measured using a clin- uals. Of these, one primer showed polymorphism. The three ometer and the aspect of the slope was measured using a primers used in the study were labelled 834 (AGA GAG AGA compass. These data were collected to assess whether sun- GAG AGA GYT), 840 (GAG AGA GAG AGA GAG AYT) light exposure has any impact on the bat populations, and 868 (GAA GAA GAA GAA GAA GAA). either directly or indirectly through its impact on the veg- It was noted that the bands on the gels being produced etation. Finally, a digital photograph was taken of the sky showed poor definition. A review of the literature indicated directly above the sample point in order to calculate the that a lower annealing temperature might be more suitable canopy cover. This was achieved using Adobe Photoshop for amplifying bat DNA. Other genetic studies of 7.0, which was first used to convert the photograph to Chiroptera have used annealing temperatures ranging from black and white, and then produced a histogram showing 29 30 45 to 528C. In an attempt to improve the quality of the the number of pixels of each colour. The number of white images, the PCR annealing temperature was therefore pixels was then divided by the total to produce a percentage changed from 56 to 448C and this change was successful. sky visibility value. For each variable, a t-test was used to PCR amplifications then began for each of the samples compare the data collected in the buffer and core zones. using each of the three suitable primers. Six cambrex flash gels were run, one for each species with Measuring Genetic Diversity each of the three primers. Photographs of the gels were taken DNA was extracted from each wing-punch using Qiagen under ultraviolet light. The band positions were then scored DNeasy kits. Briefly, 180 ml of buffer ATL (a tissue lysis using Kodak Digital Science Program, which produced a list buffer), along with 20 ml of proteinase K was added to the of molecular weights for the bands present for each individ- wing-punch and incubated at 568C for 1 h, until the ual based on known molecular weights of reference DNA. tissue was completely lysed. Two hundred microlitres of These data were then transferred into Microsoft Excel and buffer AL (a lysis buffer for DNA purification) and 200 ml analysed, scoring each individual for the presence or of ethanol (95%) were then added and the mixture pipetted absence of each band. The results of this were entered into into a DNeasy mini spin column. This column was centri- Popgene, which calculated percentage of polymorphism, fuged at 8000 rpm for 1 min, and the flow-through dis- Nei’s diversity index, Shannon–Weiner index for each carded. Next, the spin column was placed into a new locus. For each species, an analysis of variance (ANOVA) collection tube and 500 ml of wash buffer AW1 was added. was performed comparing both Nei’s and Shannon– Centrifugation was then repeated and the flow-through dis- Weiner diversity in the core and buffer zones. carded. Next, 500 ml of wash buffer AW2 was added and the column was centrifuged at 13 000 rpm for 3 min. The Results and Discussion flow-through was discarded and the spin column placed in a new collection tube. One hundred microlitres of elution To investigate whether the habitat differed between the core buffer (AE) was added and the mixture was incubated at and buffer zones, I estimated a number of habitat variables ......................................................................................................................................................................................................................................... 150 Bioscience Horizons † Volume 2 † Number 2 † June 2009 Research article ......................................................................................................................................................................................................................................... around the four mist-netting sites. I found that FHD and in genetic diversity between the buffer and core zones as fruit availability (Fig. 2) were significantly greater in the measured by Nei’s diversity index or Shannon–Weiner buffer zone sites than the core zone sites. However, it is poss- index (Fig. 4). ible that these differences were due to differences in the slope The habitat sampling in this study was relatively superficial, angle of the two collecting sites, since these also differ signifi- especially the assessment of fruit availability, which used only cantly in the 20 m radius around the mist-netting sites a very course measure. However, the sample size achieved was (Fig. 3). relatively large and was therefore able to detect differences Given that there do appear to be differences in the habitat between the two sites. The use of a circular plot from which of the core and buffer zones, we might expect there to be habitat samples were drawn has the benefit of using a single differences in the population sizes that each zone can dimension to define the perimeter of the sample area, sustain, and therefore differences in the level of genetic diver- making it easy to establish. However, one disadvantage sity. However, I found no evidence to support this conjec- with the method used in this study is that the density of ture, as neither species showed any significant differences sample points within the 40 m radius is much higher in the middle. The use of a square plot with randomly generated coordinates would not suffer from this problem and may have provided a better method for sampling the area. For the genetic data, I was only able to collect a very small sample size, due to the logistical difficulties of transporting DNA equipment to a remote field site. The data presented in this paper are therefore a very crude representation of the total genetic diversity of bat populations in Cusuco National Park, and it is quite plausible that the absence of a significant result is due to this. However, one success of this project is that I was able to perform genetic analysis in the field, where it was not possible to refrigerate DNA or enzymes. If there is in fact no difference in genetic diversity between bat populations in the buffer and core zones, there are a number of possible explanations for this result. The effect of habitat destruction on animal populations is likely to show a 32, 33 lag, although it is not clear how long this might be. One study found that population decline in Caribou showed a 20-year lag behind disturbance, while another study Figure 2. Foliage height diversity and fruit availability in buffer and core found a lag of just 1–4 years between disturbance and lek zone sites +SEM. Figure 4. Nei’s diversity and Shannon–Weiner index for S. ludovici and Figure 3. Slope angle in buffer and core zone sites +SEM. A. toltecus in buffer and core zone sites +SEM. ......................................................................................................................................................................................................................................... 151 Research article Bioscience Horizons † Volume 2 † Number 2 † June 2009 ......................................................................................................................................................................................................................................... disappearance in greater sage-grouse. The village of Buenos S. ludovici and A. toltecus in the buffer and core zones of Aires was established in 1921, before which the area is Cusuco National Park. believed to have been fully forested. The majority of the dis- Finally, the non-significant result of this study may rep- turbance in the area occurred between 1936 and 1954, resent a real absence of differences in genetic diversity during which time logging was undertaken around Buenos between the core and buffer zones because habitat disturb- Aires and the south east of the park. Cusuco National Park ance in the buffer zone is not having a significant effect on was established in 1959, preventing any further disturbance populations of S. ludovici and A. toltecus. The suggestion within the core zone and limiting destruction within the buffer that both S. ludovici and A. toltecus may be able to maintain zone to shaded coffee plantations. Thus, it is likely that dis- healthy populations within disturbed forest is congruent with turbance of some degree has been occurring for 70 years the results of some other studies. For instance, one study and that conditions should have remained relatively similar found that members of the genus Artibeus, Sturnira and for the last 40 years. From the limited data available, it Demanura are common in both pristine forest and shaded seems likely that the impact of human activities should be coffee plantations. Several authors have attributed this to evident in the bat populations now. generalist habits, which allow foraging in a variety of habi- 10, 14 Another possible explanation for the result is that the two tats. Furthermore, one study found that even species sample sites do not represent distinct populations and that with specialist foraging and roosting requirements, such as substantial gene flow is occurring maintaining genetic diver- S. ludovici, may cope well with disturbed habitats. sity at a relatively constant level. Alternatively, bats caught Research indicates that some species may actually do within the buffer zone may actually be roosting in the core better in secondary forest. In particular, Estrada et al. zone, so they represent the same population as that found found that A. toltecus was most common in shaded coffee in the core zone. Investigations into the home range size of plantations. This may be explained by the greater availability Neotropical bats have been fairly limited. However, studies of fruiting plants and trees found in disturbed forest, which that have been conducted indicate that most phyllostomid is corroborated by the significantly higher fruit availability in bat species have home ranges of just a few kilometres the buffer zone found in this study. Fruit availability may around their roost sites. One study looking at home also be more continuous in secondary forest, as successional range size for nine phyllostomid bats found that they range trees have longer fruiting periods and smaller daily crops. 2, 37 from 0.07 to 1.15 km and other studies have found However, there is substantial evidence to suggest that not 7, 38 similar results. all bat species are so tolerant of habitat disturbance. In The distance between the two sites in my study is 6 km, general, species that are abundant in pristine forest have and so based on the limited data available, it seems reasonable been found to cope well or even thrive in secondary forest, to conclude that bats caught in the buffer and core zones rep- but less common species may be more vulnerable to habitat resent samples from two, at least partially independent popu- changes. Furthermore, a study in Guatemala found that lations. However, one study on Artibeus jamaicensis found small frugivores were captured most often in fragmented that it can fly up to 8 km to forage. It is not clear whether forest where there was a high availability of small-fruited suc- home ranges of this size are wide-spread among Neotropical cessional plants, whereas larger frugivores were most bats, and whether either S. ludovici or A. toltecus are likely common in continuous forest as they required larger fruits to have home ranges this large. Only a direct investigation of unique to this habitat. Thus, dietary preferences may signifi- the home ranges of the two species used in this study can con- cantly impact on the ability of frugivorous bats to inhabit sec- clusively determine whether the buffer zone and core zone ondary forest. This is contrary to the expectation that roosting samples represent distinct populations. requirements would represent the most limiting factor in According to population genetic theory, a single migrating terms of bat abundance in disturbed habitat. individual per generation is sufficient to homogenize popu- It is important to consider that shaded coffee plantations lations. It seems likely that this level of migration could represent a relatively low-level disturbance, when compared be occurring between the populations in the buffer and with other practices such as logging. They commonly retain core zones. The result of genetic analyses can often be used the original canopy of trees as shade for the coffee plants, to calculate the level of gene flow between populations and as such, canopy species may be particularly unaffected using statistics such as F . However, this is particularly pro- by their presence. Shaded coffee plantations also contain ST blematic for dominant markers, such as ISSR markers used high plant diversity and a complex vertical vegetation struc- 40 14 in this study. Estimating the F for populations requires ture similar to that found in pristine forest. A mild effect ST that allele frequencies can be inferred, which is not possible of shaded coffee plantations on bat populations is supported with dominant markers, because dominant homozyogotes by the finding that traditional coffee plantations in Mexico cannot be distinguished from heterozygotes. As such it support a similar level of bat species diversity as in pristine has not been possible to use statistical tests to analyse the forest. More severe disturbance of the habitat would be level of migration occurring between populations of expected to have a significant effect on bat populations. ......................................................................................................................................................................................................................................... 152 Bioscience Horizons † Volume 2 † Number 2 † June 2009 Research article ......................................................................................................................................................................................................................................... The data presented in this paper are insufficient to References conclude whether shaded coffee plantations are having a 1. Laurance WF (1999) Reflections on tropical deforestation crisis. Biol Conserv significant impact on bat species in Cusuco National 91: 109–117. Park. 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Ecology 42: terns of Macrophyllum macrophyllum (Phyllostomidae) foraging over water. 594–598. J Mammal 86: 587–598. 29. Ibanez C, Garcia-Mudarra JL, Ruedi M et al. (2006) The Iberian contribution to 38. Kalko EKV, Handley CO (2001) Neotropical bats in the canopy: diversity, cryptic diversity in European bats. Acta Chiropterol 8: 277–297. community structure and implications for conservation. Vegetatio 153: 30. Piaggio AJ, Valdez EW, Boga MA et al. (2002) Systematics of Myotis occultus 319–333. (Chiroptera: Vespertilonidae) inferred from sequences of two mitochondrial 39. Hartl DL, Clark AG (1997) Principles of Population Genetics, 3rd edition. genes. Journal of Mammalogy 83: 386–395. Sunderland, MA: Sinauer Associates. 31. Newton A (2007) Forest Ecology and Conservation. Oxford: Oxford University 40. Culley TM (2005) Population Genetic Analysis of ISSR Data. http:// Press. www.biology.uc.edu/faculty/culley/Protocols/Population%20Genetic%20 32. Gu W, Heikkila R, Hanski I (2002) Estimating the consequences of habitat Analysis%20of%20ISSR%20Data.pdf (accessed 12 April 2008). fragmentation on extinction risk in dynamic landscapes. Landscape Ecol 41. Schulze MD, Seavet NE, Whitacre DF (2000) A comparison of the phyllosto- 17: 699–710. mid bat assemblages in undisturbed neotropical forest and in forest frag- 33. Bulman CR, Wilson RJ, Holt AR et al. (2007) Minimum viable metapopulation ments of a slash-and-burn farming mosaic in Peten, Guatemala. Biotropica size, extinction debt, and the conservation of a declining species. Ecol Appl 32; 174–184. 17: 1460–1473. Author Biography Claire Asher has recently graduated from the University of Sussex with a first-class degree in Biology. She also received the John Maynard Smith award for the best performance in evolutionary biology. Claire’s particular fields of interest are evolutionary theory, conservation genetics and animal behaviour. She began an MSc in Evolutionary and Behaviour ecology at the University of Exeter in October 2008, and intends to do a PhD in the future. Ultimately, Claire aims to become a research scientist studying evolution and genetics. ........................................................................................................................................................................................................................................ Submitted on 30 September 2008; accepted on 18 December 2008; advance access publication 19 April 2009 .........................................................................................................................................................................................................................................
Bioscience Horizons – Oxford University Press
Published: Jun 19, 2009
Keywords: Key words genetic diversity bat cloud forest conservation habitat disturbance
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