Chris J. Kettle

Identifying the early genetic consequences of habitat degradation in a highly threatened tropical conifer, Araucaria nemorosa Laubenfels

The early genetic effects of habitat degradation were investigated in the critically endangered conifer Araucaria nemorosa. This species occurs in New Caledonia, a global biodiversity hotspot where the worlds greatest concentration of endemic conifer species coincides with an extremely high level of habitat destruction due to fire and mining. Using seven microsatellite loci, estimates were made of genetic marker variation, inbreeding coefficients and population differentiation of adult and seedling cohorts of A. nemorosa. These were contrasted with equivalent estimates, made over similar spatial scales and with the same marker loci, in the locally common and more widespread sister species Araucaria columnaris. There were no significant differences in population genetic parameters between adult populations of the two species, despite their different abundances. However, in A. nemorosa, the juvenile cohort showed a loss of rare alleles and elevated levels of inbreeding when compared to the adult cohort. These genetic differences between the cohorts were not observed in the locally common A. columnaris. This suggests that recent environmental degradation is influencing the genetic structure of A. nemorosa populations. Although this is not detectable among predisturbance adult populations, an early warning of these impacts is evident in more recently established seedling cohorts. The conservation implications of these results are discussed.

Ecological considerations for using dipterocarps for restoration of lowland rainforest in Southeast Asia

The lowland dipterocarp forests of Southeast Asia support a substantial proportion of the world’s biodiversity. They are of considerable environmental and economic value at the local, regional and global scale, providing many goods and services to a growing population. The forests of this region are among the fastest disappearing in the world and restoration is urgently required. This paper provides a review of the ecological constraints to restoration of lowland dipterocarp forest in Southeast Asia. It focuses on the production of planting stock, the significance of site-species matching and post-planting site maintenance. It identifies gaps in our knowledge and highlights priority areas of research. Adopting a long-term view is essential for restoring as well as conserving the dipterocarp forests of Southeast Asia. An immediate strategy for the conservation and management of dwindling genetic resources of these important timber species is essential. This will provide the foundations for sourcing seed and production of planting material for longer term restoration. The importance of species-site matching, mycorrhizal fungi and post-planting maintenance for restoration are apparent. Financing is a major limiting factor to dipterocarp forest restoration. Trading in carbon, private finance and environmental markets afford considerable opportunities for restoring these forests providing their total value is recognised. Despite the wealth of ecological knowledge we already have for scientifically-informed forest restoration, without the backing of governments and corporate stakeholders, forest restoration will not gain the urgently required momentum.

Does long‐distance pollen dispersal preclude inbreeding in tropical trees? Fragmentation genetics of Dysoxylum malabaricum in an agro‐forest landscape

Tropical trees often display long‐distance pollen dispersal, even in highly fragmented landscapes. Understanding how patterns of spatial isolation influence pollen dispersal and interact with background patterns of fine‐scale spatial genetic structure (FSGS) is critical for evaluating the genetic consequences of habitat fragmentation. In the endangered tropical timber tree Dysoxylum malabaricum (Meliaceae), we apply eleven microsatellite markers with paternity and parentage analysis to directly estimate historic gene flow and contemporary pollen dispersal across a large area (216 km2) in a highly fragmented agro‐forest landscape. A comparison of genetic diversity and genetic structure in adult and juvenile life stages indicates an increase in differentiation and FSGS over time. Paternity analysis and parentage analysis demonstrate high genetic connectivity across the landscape by pollen dispersal. A comparison between mother trees in forest patches with low and high densities of adult trees shows that the frequency of short‐distance mating increases, as does average kinship among mates in low‐density stands. This indicates that there are potentially negative genetic consequences of low population density associated with forest fragmentation. Single isolated trees, in contrast, frequently receive heterogeneous pollen from distances exceeding 5 km. We discuss the processes leading to the observed patterns of pollen dispersal and the implications of this for conservation management of D. malabaricum and tropical trees more generally.

Forest fragmentation genetics in a formerly widespread island endemic tree: Vateriopsis seychellarum (Dipterocarpaceae)

Habitat fragmentation and changed land use have seriously reduced population size in many tropical forest tree species. Formerly widespread species with limited gene flow may be particularly vulnerable to the negative genetic effects of forest fragmentation and small population size. Vateriopsis seychellarum (Dipterocarpaceae) is a formerly widespread canopy tree of the Seychelles, but is now reduced to 132 adult individuals distributed in eleven sites. Using ten microsatellite loci, a genetic inventory of all adult trees and a sample of 317 progeny, we demonstrate that despite its restricted range, overall genetic diversity was relatively high (HE: 0.56). The juvenile cohort, however, had significantly lower allelic richness (adults RS: 3.91; juveniles RS: 2.83) and observed heterozygosity than adult trees (adults HO: 0.62; juveniles HO: 0.48). Rare alleles were fewer and kinship between individuals was stronger in juveniles. Significant fine‐scale spatial genetic structure was observed in remnant adults, and parentage analysis indicated that more than 90% of sampled progeny disperse <25 m and pollen dispersed <50 m. The molecular data confirmed that two populations were derived entirely from self‐fertilized offspring from a single surviving mother tree. These populations produce viable offspring. Despite this extreme genetic bottleneck, self‐compatibility may provide V. seychellarum with some resistance to the genetic consequences of habitat fragmentation, at least in the short term. We discuss our findings in the context of other rare and threatened dipterocarp species which are vulnerable to miss‐management of genetic resources and population fragmentation.

Back from the brink: potential for genetic rescue in a critically endangered tree.

Rare plant species are vulnerable to genetic erosion and inbreeding associated with small population size and isolation due to increasing habitat fragmentation. The degree to which these problems undermine population viability remains debated. We explore genetic and reproductive processes in the critically endangered long‐lived tropical tree Medusagyne oppositifolia, an endemic to the Seychelles with a naturally patchy distribution. This species is failing to recruit in three of its four populations. We evaluate whether recruitment failure is linked to genetic problems associated with fragmentation, and if genetic rescue can mitigate such problems. Medusagyne oppositifolia comprises 90 extant trees in four populations, with only the largest (78 trees) having successful recruitment. Using 10 microsatellite loci, we demonstrated that genetic diversity is high (HE: 0.48–0.63; HO: 0.56–0.78) in three populations, with only the smallest population having relatively low diversity (HE: 0.26 and HO: 0.30). All populations have unique alleles, high genetic differentiation, and significant within population structure. Pollen and seed dispersal distances were mostly less than 100 m. Individuals in small populations were more related than individuals in the large population, thus inbreeding might explain recruitment failure in small populations. Indeed, inter‐population pollination crosses from the large donor population to a small recipient population resulted in higher reproductive success relative to within‐population crosses. Our study highlights the importance of maintaining gene flow between populations even in species that have naturally patchy distributions. We demonstrate the potential for genetic and ecological rescue to support conservation of plant species with limited gene flow.

Patterns of Genetic Variation across Altitude in Three Plant Species of Semi-Dry Grasslands

Background Environmental gradients caused by altitudinal gradients may affect genetic variation within and among plant populations and inbreeding within populations. Populations in the upper range periphery of a species may be important source populations for range shifts to higher altitude in response to climate change. In this study we investigate patterns of population genetic variation at upper peripheral and lower more central altitudes in three common plant species of semi-dry grasslands in montane landscapes. Methodology/Principal Findings In Briza media, Trifolium montanum and Ranunculus bulbosus genetic diversity, inbreeding and genetic relatedness of individuals within populations and genetic differentiation among populations was characterized using AFLP markers. Populations were sampled in the Swiss Alps at 1800 (upper periphery of the study organisms) and at 1200 m a.s.l. Genetic diversity was not affected by altitude and only in B. media inbreeding was greater at higher altitudes. Genetic differentiation was slightly greater among populations at higher altitudes in B. media and individuals within populations were more related to each other compared to individuals in lower altitude populations. A similar but less strong pattern of differentiation and relatedness was observed in T. montanum, while in R. bulbosus there was no effect of altitude. Estimations of population size and isolation of populations were similar, both at higher and lower altitudes. Conclusions/Significance Our results suggest that altitude does not affect genetic diversity in the grassland species under study. Genetic differentiation of populations increased only slightly at higher elevation, probably due to extensive (historic) gene flow among altitudes. Potentially pre-adapted genes might therefore spread easily across altitudes. Our study indicates that populations at the upper periphery are not genetically depauperate or isolated and thus may be important source populations for migration under climate change.

Ecological implications of a flower size/number trade-off in tropical forest trees

Background In angiosperms, flower size commonly scales negatively with number. The ecological consequences of this trade-off for tropical trees remain poorly resolved, despite their potential importance for tropical forest conservation. We investigated the flower size number trade-off and its implications for fecundity in a sample of tree species from the Dipterocarpaceae on Borneo. Methodology/Principal Findings We combined experimental exclusion of pollinators in 11 species, with direct and indirect estimates of contemporary pollen dispersal in two study species and published estimates of pollen dispersal in a further three species to explore the relationship between flower size, pollinator size and mean pollen dispersal distance. Maximum flower production was two orders of magnitude greater in small-flowered than large-flowered species of Dipterocarpaceae. In contrast, fruit production was unrelated to flower size and did not differ significantly among species. Small-flowered species had both smaller-sized pollinators and lower mean pollination success than large-flowered species. Average pollen dispersal distances were lower and frequency of mating between related individuals was higher in a smaller-flowered species than a larger-flowered confamilial. Our synthesis of pollen dispersal estimates across five species of dipterocarp suggests that pollen dispersal scales positively with flower size. Conclusions and Their Significance Trade-offs embedded in the relationship between flower size and pollination success contribute to a reduction in the variance of fecundity among species. It is therefore plausible that these processes could delay competitive exclusion and contribute to maintenance of species coexistence in this ecologically and economically important family of tropical trees. These results have practical implications for tree species conservation and restoration. Seed collection from small-flowered species may be especially vulnerable to cryptic genetic erosion. Our findings also highlight the potential for differential vulnerability of tropical tree species to the deleterious consequences of forest fragmentation.

Extensive contemporary pollen-mediated gene flow in two herb species, Ranunculus bulbosus and Trifolium montanum, along an altitudinal gradient in a meadow landscape

BACKGROUND AND AIMS Genetic connectivity between plant populations allows for exchange and dispersal of adaptive genes, which can facilitate plant population persistence particularly in rapidly changing environments. METHODS Patterns of historic gene flow, flowering phenology and contemporary pollen flow were investigated in two common herbs, Ranunculus bulbosus and Trifolium montanum, along an altitudinal gradient of 1200-1800 m a.s.l. over a distance of 1 km among five alpine meadows in Switzerland. KEY RESULTS Historic gene flow was extensive, as revealed by Fst values of 0·01 and 0·007 in R. bulbosus and T. montanum, respectively, by similar levels of allelic richness among meadows and by the grouping of all individuals into one genetic cluster. Our data suggest contemporary pollen flow is not limited across altitudes in either species but is more pronounced in T. montanum, as indicated by the differential decay of among-sibships correlated paternity with increasing spatial distance. Flowering phenology among meadows was not a barrier to pollen flow in T. montanum, as the large overlap between meadow pairs was consistent with the extensive pollen flow. The smaller flowering overlap among R. bulbosus meadows might explain the slightly more limited pollen flow detected. CONCLUSIONS High levels of pollen flow among altitudes in both R. bulbosus and T. montanum should facilitate exchange of genes which may enhance adaptive responses to rapid climate change.

Forest trees in human modified landscapes: ecological and genetic drivers of recruitment failure in Dysoxylum malabaricum (Meliaceae).

Tropical agro-forest landscapes are global priority areas for biodiversity conservation. Little is known about the ability of these landscapes to sustain large late successional forest trees upon which much forest biodiversity depends. These landscapes are subject to fragmentation and additional habitat degradation which may limit tree recruitment and thus compromise numerous ecosystem services including carbon storage and timber production. Dysoxylum malabaricum is a large canopy tree species in the Meliaceae, a family including many important tropical timber trees. This species is found in highly fragmented forest patches within a complex agro-forest landscape of the Western Ghats biodiversity hot spot, South India. In this paper we combined a molecular assessment of inbreeding with ecological and demographic data to explore the multiple threats to recruitment of this tree species. An evaluation of inbreeding, using eleven microsatellite loci in 297 nursery-reared seedlings collected form low and high density forest patches embedded in an agro-forest matrix, shows that mating between related individuals in low density patches leads to reduced seedling performance. By quantifying habitat degradation and tree recruitment within these forest patches we show that increasing canopy openness and the increased abundance of pioneer tree species lead to a general decline in the suitability of forest patches for the recruitment of D. malabaricum. We conclude that elevated inbreeding due to reduced adult tree density coupled with increased degradation of forest patches, limit the recruitment of this rare late successional tree species. Management strategies which maintain canopy cover and enhance local densities of adult trees in agro-forest mosaics will be required to ensure D. malabaricum persists in these landscapes. Our study highlights the need for a holistic understanding of the incipient processes that threaten populations of many important and rare tropical tree species in human dominated agro-forest landscapes.

Fragmentation Genetics of Vateria indica: implications for management of forest genetic resources of an endemic dipterocarp

Tropical agro-forest landscapes are potentially valuable reserves of forest genetic resources for forestry and restoration of degraded forests. The Dipterocarpaceae is a dominant Southeast Asian family of tree species of global significance for the tropical timber industry. Very little information exists about how effective human modified landscapes are for conserving genetic diversity in dipterocarp species. This study provides a baseline for understanding how fragmented agro-forest landscapes in India sustain forest genetic resources in an endemic dipterocarp tree. We compare genetic diversity and fine-scale spatial genetic structure (FSGS) in the threatened tree species Vateria indica within an isolated and a continuous forest site in the Western Ghats, South India. We place these results in the context of dipterocarps from both the Seychelles and Borneo. Parentage analysis of 694 progeny using twelve nuclear microsatellite markers is applied to estimate pollen and seed dispersal. Using a nursery trial we evaluate effects of inbreeding on growth performance. Our results show that levels of FSGS, and gene dispersal are comparable between a small isolated and a large continuous site of V. indica. Realized long-distance pollen flow into the isolated patch appears to help maintaining genetic diversity. The nursery experiment suggests that selection favours outbred progeny. Individuals of V. indica in close proximity appear less related to each other than in another highly fragmented and endangered dipterocarp species from the Seychelles, but more related than in three dipterocarp species studied in continuous forest in Borneo. We discuss the wider implications of our findings in the context of conservation and restoration of dipterocarp forest genetic resources in fragmented populations.