The effects of habitat fragmentation on the demography and population genetic structure of Uromys Caudimaculatus

Habitat fragmentation can have an impact on a wide variety of biological processes including abundance, life history strategies, mating system, inbreeding and genetic diversity levels of individual species. Although fragmented populations have received much attention, ecological and genetic responses of species to fragmentation have still not been fully resolved. The current study investigated the ecological factors that may influence the demographic and genetic structure of the giant white-tailed rat (Uromys caudimaculatus) within fragmented tropical rainforests. It is the first study to examine relationships between food resources, vegetation attributes and Uromys demography in a quantitative manner. Giant white-tailed rat densities were strongly correlated with specific suites of food resources rather than forest structure or other factors linked to fragmentation (i.e. fragment size). Several demographic parameters including the density of resident adults and juvenile recruitment showed similar patterns. Although data were limited, high quality food resources appear to initiate breeding in female Uromys. Where data were sufficient, influx of juveniles was significantly related to the density of high quality food resources that had fallen in the previous three months. Thus, availability of high quality food resources appear to be more important than either vegetation structure or fragment size in influencing giant white-tailed rat demography. These results support the suggestion that a species’ response to fragmentation can be related to their specific habitat requirements and can vary in response to local ecological conditions. In contrast to demographic data, genetic data revealed a significant negative effect of habitat fragmentation on genetic diversity and effective population size in U. caudimaculatus. All three fragments showed lower levels of allelic richness, number of private alleles and expected heterozygosity compared with the unfragmented continuous rainforest site. Populations at all sites were significantly differentiated, suggesting restricted among population gene flow. The combined effects of reduced genetic diversity, lower effective population size and restricted gene flow suggest that long-term viability of small fragmented populations may be at risk, unless effective management is employed in the future. A diverse range of genetic reproductive behaviours and sex-biased dispersal patterns were evident within U. caudimaculatus populations. Genetic paternity analyses revealed that the major mating system in U. caudimaculatus appeared to be polygyny at sites P1, P3 and C1. Evidence of genetic monogamy, however, was also found in the three fragmented sites, and was the dominant mating system in the remaining low density, small fragment (P2). High variability in reproductive skew and reproductive success was also found but was less pronounced when only resident Uromys were considered. Male body condition predicted which males sired offspring, however, neither body condition nor heterozygosity levels were accurate predictors of the number of offspring assigned to individual males or females. Genetic spatial autocorrelation analyses provided evidence for increased philopatry among females at site P1, but increased philopatry among males at site P3. This suggests that male-biased dispersal occurs at site P1 and female-biased dispersal at site P3, implying that in addition to mating systems, Uromys may also be able to adjust their dispersal behaviour to suit local ecological conditions. This study highlights the importance of examining the mechanisms that underlie population-level responses to habitat fragmentation using a combined ecological and genetic approach. The ecological data suggested that habitat quality (i.e. high quality food resources) rather than habitat quantity (i.e. fragment size) was relatively more important in influencing giant white-tailed rat demographics, at least for the populations studied here . Conversely, genetic data showed strong evidence that Uromys populations were affected adversely by habitat fragmentation and that management of isolated populations may be required for long-term viability of populations within isolated rainforest fragments.

Evolutionary biology of Gondwanan non-biting midges (Diptera: Chironomidae)

The potential restriction to effective dispersal and gene flow caused by habitat fragmentation can apply to multiple levels of evolutionary scale; from the fragmentation of ancient supercontinents driving diversification and speciation on disjunct landmasses, to the isolation of proximate populations as a result of their inability to cross intervening unsuitable habitat. Investigating the role of habitat fragmentation in driving diversity within and among taxa can thus include inferences of phylogenetic relationships among taxa, assessments of intraspecific phylogeographic structure and analyses of gene flow among neighbouring populations. The proposed Gondwanan clade within the chironomid (non-biting midge) subfamily Orthocladiinae (Diptera: Chironomidae) represents a model system for investigating the role that population fragmentation and isolation has played at different evolutionary scales. A pilot study by Krosch et al (2009) indentified several highly divergent lineages restricted to ancient rainforest refugia and limited gene flow among proximate sites within a refuge for one member of this clade, Echinocladius martini Cranston. This study provided a framework for investigating the evolutionary history of this taxon and its relatives more thoroughly. Populations of E. martini were sampled in the Paluma bioregion of northeast Queensland to investigate patterns of fine-scale within- and among-stream dispersal and gene flow within a refuge more rigorously. Data was incorporated from Krosch et al (2009) and additional sites were sampled up- and downstream of the original sites. Analyses of genetic structure revealed strong natal site fidelity and high genetic structure among geographically proximate streams. Little evidence was found for regular headwater exchange among upstream sites, but there was distinct evidence for rare adult flight among sites on separate stream reaches. Overall, however, the distribution of shared haplotypes implied that both larval and adult dispersal was largely limited to the natal stream channel. Patterns of regional phylogeographic structure were examined in two related austral orthoclad taxa – Naonella forsythi Boothroyd from New Zealand and Ferringtonia patagonica Sæther and Andersen from southern South America – to provide a comparison with patterns revealed in their close relative E. martini. Both taxa inhabit tectonically active areas of the southern hemisphere that have also experienced several glaciation events throughout the Plio-Pleistocene that are thought to have affected population structure dramatically in many taxa. Four highly divergent lineages estimated to have diverged since the late Miocene were revealed in each taxon, mirroring patterns in E. martini; however, there was no evidence for local geographical endemism, implying substantial range expansion post-diversification. The differences in pattern evident among the three related taxa were suggested to have been influenced by variation in the responses of closed forest habitat to climatic fluctuations during interglacial periods across the three landmasses. Phylogeographic structure in E. martini was resolved at a continental scale by expanding upon the sampling design of Krosch et al (2009) to encompass populations in southeast Queensland, New South Wales and Victoria. Patterns of phylogeographic structure were consistent with expectations and several previously unrecognised lineages were revealed from central- and southern Australia that were geographically endemic to closed forest refugia. Estimated divergence times were congruent with the timing of Plio-Pleistocene rainforest contractions across the east coast of Australia. This suggested that dispersal and gene flow of E. martini among isolated refugia was highly restricted and that this taxon was susceptible to the impacts of habitat change. Broader phylogenetic relationships among taxa considered to be members of this Gondwanan orthoclad group were resolved in order to test expected patterns of evolutionary affinities across the austral continents. The inferred phylogeny and estimated divergence times did not accord with expected patterns based on the geological sequence of break-up of the Gondwanan supercontinent and implied instead several transoceanic dispersal events post-vicariance. Difficulties in appropriate taxonomic sampling and accurate calibration of molecular phylogenies notwithstanding, the sampling regime implemented in the current study has been the most intensive yet performed for austral members of the Orthocladiinae and unsurprisingly has revealed both novel taxa and phylogenetic relationships within and among described genera. Several novel associations between life stages are made here for both described and previously unknown taxa. Investigating evolutionary relationships within and among members of this clade of proposed Gondwanan orthoclad taxa has demonstrated that a complex interaction between historical population fragmentation and dispersal at several levels of evolutionary scale has been important in driving diversification in this group. While interruptions to migration, colonisation and gene flow driven by population fragmentation have clearly contributed to the development and maintenance of much of the diversity present in this group, long-distance dispersal has also played a role in influencing diversification of continental biotas and facilitating gene flow among disjunct populations.

Isolation and characterisation of novel microsatellite and mitochondrial DNA markers for the Eastern Water Dragon (Physignathus lesueurii)

Habitat fragmentation as a result of urbanisation is a growing problem for native lizard species. The Eastern Water Dragon (Physignathus lesueurii) is a social arboreal agamid lizard, native to Australia. This species represents an ideal model species to investigate the effect of urbanisation because of their prominent abundance in the urban landscape. Here we describe the isolation and characterisation of a novel set of 74 di-, tri-, and tetramicrosatellites from which 18 were selected and optimised into two multiplexes. The 18 microsatellites generated a total 148 alleles across the two populations. The number of alleles per locus varied from 2 to 18 alleles and measures of Ho and He varied from 0.395 to 0.877 and from 0.441 to 0.880, respectively. We also present primers for four novel mitochondrial DNA (mtDNA) markers. The combined length of the four mtDNA marker pairs was 2,528 bp which included 15 nucleotides changes. In comparison to threatened species, which are generally characterised by small population sizes, the Eastern Water Dragon represents an ideal model species to investigate the effect of urbanisation on their behavioural ecology and connectivity patterns among populations.

Phylogeography of Echinocladius martini Cranston (Diptera: Chironomidae) in closed forest streams of eastern Australia

The eastern Australian rainforests have experienced several cycles of range contraction and expansion since the late Miocene that are closely correlated with global glaciation events. Together with ongoing aridification of the continent, this has resulted in current distributions of native closed forest that are highly fragmented along the east coast. Several closed forest endemic taxa exhibit patterns of population genetic structure that are congruent with historical isolation of populations in discrete refugia and reflect evolutionary histories dramatically affected by vicariance. Currently, limited data are available regarding the impact of these past climatic fluctuations on freshwater invertebrate taxa. The non-biting midge species Echinocladius martini Cranston is distributed along the east coast and inhabits predominantly montane streams in closed forest habitat. Phylogeographic structure in E. martini was resolved here at a continental scale by incorporating data from a previous pilot study and expanding the sampling design to encompass populations in the Wet Tropics of north-eastern Queensland, south-east Queensland, New South Wales and Victoria. Patterns of phylogeographic structure revealed several deeply divergent mitochondrial lineages from central and south-eastern Australia that were previously unrecognised and were geographically endemic to closed forest refugia. Estimated divergence times were congruent with late Miocene onset of rainforest contractions across the east coast of Australia. This suggested that dispersal and gene flow among E. martini populations isolated in refugia has been highly restricted historically. Moreover, these data imply, in contrast to existing preconceptions about freshwater invertebrates, that this taxon may be acutely susceptible to habitat fragmentation.

Anthropogenic landscape change promotes asymmetric dispersal and limits regional patch occupancy in a spatially structured bird population

1. Local extinctions in habitat patches and asymmetric dispersal between patches are key processes structuring animal populations in heterogeneous environments. Effective landscape conservation requires an understanding of how habitat loss and fragmentation influence demographic processes within populations and movement between populations. 2. We used patch occupancy surveys and molecular data for a rainforest bird, the logrunner (Orthonyx temminckii), to determine (i) the effects of landscape change and patch structure on local extinction; (ii) the asymmetry of emigration and immigration rates; (iii) the relative influence of local and between-population landscapes on asymmetric emigration and immigration; and (iv) the relative contributions of habitat loss and habitat fragmentation to asymmetric emigration and immigration. 3. Whether or not a patch was occupied by logrunners was primarily determined by the isolation of that patch. After controlling for patch isolation, patch occupancy declined in landscapes experiencing high levels of rainforest loss over the last 100 years. Habitat loss and fragmentation over the last century was more important than the current pattern of patch isolation alone, which suggested that immigration from neighbouring patches was unable to prevent local extinction in highly modified landscapes. 4. We discovered that dispersal between logrunner populations is highly asymmetric. Emigration rates were 39% lower when local landscapes were fragmented, but emigration was not limited by the structure of the between-population landscapes. In contrast, immigration was 37% greater when local landscapes were fragmented and was lower when the between-population landscapes were fragmented. Rainforest fragmentation influenced asymmetric dispersal to a greater extent than did rainforest loss, and a 60% reduction in mean patch area was capable of switching a population from being a net exporter to a net importer of dispersing logrunners. 5. The synergistic effects of landscape change on species occurrence and asymmetric dispersal have important implications for conservation. Conservation measures that maintain large patch sizes in the landscape may promote asymmetric dispersal from intact to fragmented landscapes and allow rainforest bird populations to persist in fragmented and degraded landscapes. These sink populations could form the kernel of source populations given sufficient habitat restoration. However, the success of this rescue effect will depend on the quality of the between-population landscapes.

Cryptic diversity and evolutionary relationships among Australian closed-forest Melomys (Rodentia: Muridae) and related Australo-Papuan mosaic-tailed rats

This thesis investigates patterns of evolution in a group of native Australo-Papuan rodents. Past climatic change and associated sea level fluctuations, and fragmentation of wet forests in eastern Australia has facilitated rapid radiation, diversification and speciation in this group. This study adds to our understanding of the evolution of Australia’s rainforest fauna and describes the evolutionary relationships of a new genus of Australian rodent.

The 10 Australian ecosystems most vulnerable to tipping points

We identify the 10 major terrestrial and marine ecosystems in Australia most vulnerable to tipping points, in which modest environmental changes can cause disproportionately large changes in ecosystem properties. To accomplish this we independently surveyed the coauthors of this paper to produce a list of candidate ecosystems, and then refined this list during a 2-day workshop. The list includes (1) elevationally restricted mountain ecosystems, (2) tropical savannas, (3) coastal floodplains and wetlands, (4) coral reefs, (5) drier rainforests, (6) wetlands and floodplains in the Murray-Darling Basin, (7) the Mediterranean ecosystems of southwestern Australia, (8) offshore islands, (9) temperate eucalypt forests, and (10) salt marshes and mangroves. Some of these ecosystems are vulnerable to widespread phase-changes that could fundamentally alter ecosystem properties such as habitat structure, species composition, fire regimes, or carbon storage. Others appear susceptible to major changes across only part of their geographic range, whereas yet others are susceptible to a large-scale decline of key biotic components, such as small mammals or stream-dwelling amphibians. For each ecosystem we consider the intrinsic features and external drivers that render it susceptible to tipping points, and identify subtypes of the ecosystem that we deem to be especially vulnerable. © 2011 Elsevier Ltd.

Linking ecological condition and the soundscape in fragmented Australian forests

Natural landscapes are increasingly subjected to anthropogenic pressure and fragmentation resulting in reduced ecological condition. In this study we examined the relationship between ecological condition and the soundscape in fragmented forest remnants of south-east Queensland, Australia. The region is noted for its high biodiversity value and increased pressure associated with habitat fragmentation and urbanisation. Ten sites defined by a distinct open eucalypt forest community dominated by spotted gum (Corymbia citriodora ssp. variegata) were stratified based on patch size and patch connectivity. Each site underwent a series of detailed vegetation condition and landscape assessments, together with bird surveys and acoustic analysis using relative soundscape power. Univariate and multivariate analyses indicated that the measurement of relative soundscape power reflects ecological condition and bird species richness, and is dependent on the extent of landscape fragmentation. We conclude that acoustic monitoring technologies provide a cost effective tool for measuring ecological condition, especially in conjunction with established field observations and recordings.

Pleistocene climate fluctuations influence phylogeographical patterns in Melomys cervinipes across the mesic forests of eastern Australia

Aim Our aim was to clarify the lineage-level relationships for Melomys cervinipes and its close relatives and investigate whether the patterns of divergence observed for these wet-forest-restricted mammals may be associated with recognized biogeographical barriers. Location Mesic closed forest along the east coast of Australia, from north Queensland to mid-eastern New South Wales. Methods To enable rigorous phylogenetic reconstruction, divergence-date estimation and phylogeographical inference, we analysed DNA sequence and microsatellite data from 307 specimens across the complete distribution of M. cervinipes (45 localities). Results Three divergent genetic lineages were found within M. cervinipes, corresponding to geographically delineated northern, central and southern clades. Additionally, a fourth lineage, comprising M. rubicola and M. capensis, was identified and was most closely related to the northern M. cervinipes lineage. Secondary contact of the northern and central lineages was identified at one locality to the north of the Burdekin Gap. Main conclusions Contemporary processes of repeated habitat fragmentation and contraction, local extinction events and subsequent re-expansion across both small and large areas, coupled with the historical influence of the Brisbane Valley Barrier, the St Lawrence Gap and the Burdekin Gap, have contributed to the present phylogeographical structure within M. cervinipes. Our study highlights the need to sample close to the periphery of putative biogeographical barriers or risk missing vital phylogeographical information that may significantly alter the interpretation of biogeographical hypotheses.

Optimal allocation of conservation effort among subpopulations of a threatened species: How important is patch quality?

Money is often a limiting factor in conservation, and attempting to conserve endangered species can be costly. Consequently, a framework for optimizing fiscally constrained conservation decisions for a single species is needed. In this paper we find the optimal budget allocation among isolated subpopulations of a threatened species to minimize local extinction probability. We solve the problem using stochastic dynamic programming, derive a useful and simple alternative guideline for allocating funds, and test its performance using forward simulation. The model considers subpopulations that persist in habitat patches of differing quality, which in our model is reflected in different relationships between money invested and extinction risk. We discover that, in most cases, subpopulations that are less efficient to manage should receive more money than those that are more efficient to manage, due to higher investment needed to reduce extinction risk. Our simple investment guideline performs almost as well as the exact optimal strategy. We illustrate our approach with a case study of the management of the Sumatran tiger, Panthera tigris sumatrae, in Kerinci Seblat National Park (KSNP), Indonesia. We find that different budgets should be allocated to the separate tiger subpopulations in KSNP. The subpopulation that is not at risk of extinction does not require any management investment. Based on the combination of risks of extinction and habitat quality, the optimal allocation for these particular tiger subpopulations is an unusual case: subpopulations that occur in higher-quality habitat (more efficient to manage) should receive more funds than the remaining subpopulation that is in lower-quality habitat. Because the yearly budget allocated to the KSNP for tiger conservation is small, to guarantee the persistence of all the subpopulations that are currently under threat we need to prioritize those that are easier to save. When allocating resources among subpopulations of a threatened species, the combined effects of differences in habitat quality, cost of action, and current subpopulation probability of extinction need to be integrated. We provide a useful guideline for allocating resources among isolated subpopulations of any threatened species. © 2010 by the Ecological Society of America.

Paying the extinction debt: Woodland birds in the Mount Lofty Ranges, South Australia

Approximately 90% of the original woodlands of the Mount Lofty Ranges of South Australia has been cleared, modified or fragmented, most severely in the last 60 years, and affecting the avifauna dependent on native vegetation. This study identifies which woodland-dependent species are still declining in two different habitats, Pink GumBlue Gum woodland and Stringybark woodland. We analyse the Mount Lofty Ranges Woodland Bird Long-Term Monitoring Dataset for 1999-2007, to look for changes in abundance of 59 species. We use logistic regression of prevalence on lists in a Bayesian framework, and List Length Analysis to control for variation in detectability. Compared with Reporting Rate Analysis, a more traditional approach, List Length Analysis provides tighter confidence intervals by accounting for changing detectability. Several common species were declining significantly. Increasers were generally large-bodied generalists. Many birds have already disappeared from this modified and naturally isolated woodland island, and our results suggest that more specialist insectivores are likely to follow. The Mount Lofty Ranges can be regarded as a 'canary landscape' for temperate woodlands elsewhere in Australia without immediate action their bird communities are likely to follow the trajectory of the Mount Lofty Ranges avifauna. Alternatively, with extensive habitat restoration and management, we could avoid paying the extinction debt. © Royal Australasian Ornithologists Union 2011.

Isolation and inheritance of microsatellite loci for the oily bittering (Acheilognathus koreensis): applications for analysis of genetic diversity of wild populations

The oily bittering Acheilognathus koreensis is a freshwater species that is endemic to Korea and is experiencing severe declines in natural populations as a result of habitat fragmentation and water pollution. For the conservation and restoration of this species, it is necessary to assess its genetic diversity at the population level. We developed 13 polymorphic microsatellite loci that were used to analyze the genetic diversity of two populations collected from the Kum River and the Tamjin River in Korea. All loci exhibited Mendelian inheritance patterns when examined in controlled crosses. Both populations revealed high levels of variability, with the number of alleles ranging from 3 to 20 and observed and expected heterozygosities ranging from 0.500 to 0.969 and from 0.529 to 0.938, respectively. None of the loci showed significant deviation from Hardy–Weinberg equilibrium, and one pair of loci showed significant linkage disequilibrium after Bonferroni correction. Pairwise F ST and genetic distance estimation showed significant differences between two populations. These results suggest that the microsatellites developed herein can be used to study the genetic diversity, population structure and conservation measure of A. koreensis.

Characterization of novel microsatellite markers derived from Korean rose bitterling (Rhodeus uyekii) genomic library

Korean rose bitterling (Rhodeus uyekii) is a freshwater fish endemic to Korea. Natural populations of this species have experienced severe declines as a result of habitat fragmentation and water pollution. To conserve and restore R. uyekii, the genetic diversity of this species needs to be assessed at the population level. Eighteen novel polymorphic microsatellite loci for R. uyekii were developed using an enriched partial genomic library. Polymorphisms at these loci were studied in 150 individuals collected from three populations. The number of alleles at each locus ranged from 3 to 47 (mean = 17.1). Within the populations, the observed heterozygosity ranged from 0.032 to 1.000, expected heterozygosity from 0.082 to 0.967, and polymorphism information content from 0.078 to 0.950. Six loci showed significant deviation from Hardy-Weinberg equilibrium after Bonferroni’s correction, and no significant linkage disequilibrium was detected between most locus pairs, except in three cases. These highly informative microsatellite markers should be useful for genetic population structure analyses of R. uyekii.

Predicting loss and fragmentation of habitat of the vulnerable subtropical rainforest tree Macadamia integrifolia with models developed from compiled ecological data

Habitat models are widely used in ecology, however there are relatively few studies of rare species, primarily because of a paucity of survey records and lack of robust means of assessing accuracy of modelled spatial predictions. We investigated the potential of compiled ecological data in developing habitat models for Macadamia integrifolia, a vulnerable mid-stratum tree endemic to lowland subtropical rainforests of southeast Queensland, Australia. We compared performance of two binomial models—Classification and Regression Trees (CART) and Generalised Additive Models (GAM)—with Maximum Entropy (MAXENT) models developed from (i) presence records and available absence data and (ii) developed using presence records and background data. The GAM model was the best performer across the range of evaluation measures employed, however all models were assessed as potentially useful for informing in situ conservation of M. integrifolia, A significant loss in the amount of M. integrifolia habitat has occurred (p < 0.05), with only 37% of former habitat (pre-clearing) remaining in 2003. Remnant patches are significantly smaller, have larger edge-to-area ratios and are more isolated from each other compared to pre-clearing configurations (p < 0.05). Whilst the network of suitable habitat patches is still largely intact, there are numerous smaller patches that are more isolated in the contemporary landscape compared with their connectedness before clearing. These results suggest that in situ conservation of M. integrifolia may be best achieved through a landscape approach that considers the relative contribution of small remnant habitat fragments to the species as a whole, as facilitating connectivity among the entire network of habitat patches.

Temporal and spatial distribution and habitat associations of an urban population of New Zealand long-tailed bats (Chalinolobus tuberculatus)

Two ultrasound survey methods were used to determine the presence and activity patterns of New Zealand long-tailed bats (Chalinolobus tuberculatus) in the city of Hamilton. First, 13 monthly surveys conducted at 18 green spaces found C. tuberculatus in only one urban forest reserve, Hammond Bush, where they were found consistently throughout the year. Bat activity was strongly related to temperature. Second, twice-yearly citywide surveys conducted over 2 years determined the distribution and habitat associations of C. tuberculatus. Bats were found only in the southern part of the city and were strongly associated with the Waikato River. Bat activity was negatively correlated with housing and street light density and positively correlated with topographical complexity. In Hamilton, topographical complexity indicates the presence of gullies. Gullies probably provide foraging and roosting opportunities and connect the river to distant forest patches. These results suggest that urban habitats can be useful for bats if gullies can link these to distant habitat fragments.