Patching up the divide: population dynamics and genetics of small mammals in a fragmented rainforest landscape
Geurts, Katrien An-Sofie (2013) Patching up the divide: population dynamics and genetics of small mammals in a fragmented rainforest landscape. PhD thesis, James Cook University.
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Abstract
The scattered rainforests of the Atherton Tablelands in north Queensland are a classic example of habitat fragmentation. Many populations of cool-adapted species occurring in this area are restricted to small fragments and their habitat is expected to shrink further with climate change. If cool-adapted species are to persist into the future they will need to have the possibility to disperse to highland refugia. This thesis: "Patching up the divide: population dynamics and genetics of small mammals in a fragmented rainforest landscape" identifies key fragmentation aspects and evaluates the potential for connectivity on a landscape-wide and a fine scale.
I measured the influence of forest configuration, patch size, connectivity and isolation age on the population structure of rainforest mammals. In continuous and fragmented rainforest tree-kangaroos and possums were surveyed by spotlighting and rodents and other small marsupials by mark-recapture techniques. Population demography of three common and abundant rodent species: Melomys cervinipes, Rattus leucopus and Uromys caudimaculatus was studied in more detail. DNA was sampled from two focal rodent species, Melomys cervinipes and Rattus leucopus, to evaluate how the mosaic nature of the landscape affected genetic variation, differentiation, relatedness and gene flow. For genetic investigations five microsatellite loci were amplified in M. cervinipes and eight loci in R. leucopus. The mitochondrial DNA D-loop was also targeted in R. leucopus. Vegetation structure surveys were conducted to reveal fine-scale variation in the habitat and its influence on population demography and genetic structure of the two main study species.
I found that non-flying mammal species diversity was greatest in continuous forest and in large fragments with few climbing palms and less ground cover, indicating that large patches can support a near complete rainforest mammal species assemblage, including fragmentation-sensitive species that were mostly absent from small patches. Abundance of the three focal rodent species decreased with decreasing patch size, significantly so for R. leucopus. Decreasing patch size may have had negative impacts on breeding rates in the three focal rodent species. The number of M. cervinipes lactating females significantly declined in smaller patches. For the largest rodent species (Uromys caudimaculatus) subadults were found only in large fragments, suggesting that this species might only breed in large fragments, this result, however, was based on small sample sizes and should be treated with caution. Sex ratio and the proportion of adults to subadults did not vary significantly with patch size in the two smaller rodent species (M. cervinipes, R. leucopus). However M. cervinipes adults and R. leucopus subadult females were in poorer body condition in small fragments, potentially indicating that small fragments contained fewer resources.
Mark recapture in fragmented and continuous forest sites revealed that most movements by M. cervinipes and R. leucopus occurred on a small scale (30-60 m). The distances moved by most individuals were shorter in small fragments compared with larger remnants and continuous forest. This effect was primarily influenced by vegetation structure, while space limitation, resource availability and mating opportunities likely played an additional role. Vegetation structural elements most influential for routine movements and dispersal behaviour of both species were: ground cover, abundance of climbing palms and canopy height. Where climbing palms were common, rodents tended to be more sedentary, while in areas with a high percentage of ground cover and canopy cover more movements occurred. It appeared that the two smallest rodents (M. cervinipes and R. leucopus) had a population demography that was well adapted for life in small fragments and that these species adjusted their foraging behaviour to suit present resource availability and mating opportunities. The larger rodent (U. caudimaculatus) could experience a lack of good-quality breeding habitat in small sites but populations seemed to persist and dispersing individuals could use these remnants as stop-over places when migrating between larger sites.
Populations of M. cervinipes and R. leucopus have maintained high genetic variation and showed no clear evidence of inbreeding. Genetic variation and relatedness were not affected by site size, but were influenced by connectivity and time since isolation. Populations in small sites may have maintained genetic variation by retaining a sufficiently large population size and by gene flow. In currently unconnected sites that had been isolated for a short period of time, lower genetic diversity and higher relatedness was found than in continuous forest, or sites previously isolated and then reconnected by riparian corridors. This demonstrated that connectivity allowed gene flow to restore and maintain genetic variation. Population genetic structure reflected both historical and recent fragmentation. Historical environmental changes from the Pleistocene could be detected in separate populations from the eastern and the western Tablelands, but recent anthropogenic impacts also influenced genetic differentiation. Population differentiation and migration rates for M. cervinipes and R. leucopus were driven by an interaction between geographic distance and connectivity but these two factors did not explain the entire complexity. Directional gene flow from smaller towards larger sites consistently occurred across the landscape in both species. It appeared that individuals were selecting against low quality habitat (in small sites) and were dispersing towards higher quality habitat (in large sites). Although many individuals were emigrating from small patches, genetic diversity in these sites remained high, indicating that even low migration rates provided a regular influx of new genetic material.
Populations of M. cervinipes had lower genetic differentiation and relatedness and higher heterozygosity compared with R. leucopus. These species also experienced barriers and fine-scale structuring of the habitat differently. Values of spatial autocorrelation for R. leucopus in small and in large fragments were on average higher than for M. cervinipes, suggesting that the former species was more restricted by fine-scale changes, for example, in vegetation structure. Differences appeared to be related to the ecology of the two species. Melomys cervinipes is a scansorial species that can climb trees with great agility. This ability expands its niche and allows it to use food resources and shelter not available to terrestrial species such as R. leucopus. It also increases the resilience of M. cervinipes to fragmentation, allowing easier movements along vegetated riparian strips with canopy connectivity but sparse understorey. In contrast, the requirement for tree cover hampers the dispersal of M. cervinipes through grassland as migration rates were lower than those of R. leucopus when sites were separated by long distances of pasture. Nevertheless migration rates for both species were, on average, low, suggesting that dispersal movements were rare events in an ecological timeframe. Therefore continued gene flow will be crucial to avoid future negative effects caused by inbreeding and genetic drift. A well-connected metapopulation can maintain both species and genetic diversity as increased heterogeneity in the landscape can support a wider variety of species and genetic drift will increase the genetic difference between populations. Small patches appeared to perform an important function in the landscape, as valuable habitat and as stepping stones across the matrix between larger patches of forest. To ensure uniform distribution of gene flow across the landscape it will be important to improve habitat quality of small fragments and matrix permeability, while accommodating individual species characteristics and requirements. Therefore genetic estimates of dispersal were combined with resistance mapping and climate refugia models to identify key rainforest patches and potential areas for corridor construction.
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