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Biodiversity and Conservation (v.21, #6)


Ex situ conservation programmes in European zoological gardens: Can we afford to lose them? by Spartaco Gippoliti (pp. 1359-1364).
The role of ex situ activities for the conservation of biodiversity, and of zoos and aquaria in particular, is open to continuing debate. The present note highlights the conservation breeding potential of zoological gardens and aquaria in the European union, but it also recognises the lack of a convincing scientific and legal framework that encourages ex situ activities for ‘exotic’ species. If ex situ programmes are considered essential for global biodiversity conservation, the EU should not limit itself to regulating zoos through the zoo directive, but should actively promote and support their ex situ conservation activities.

Keywords: Biodiversity convention; Zoos; Breeding facilities; Reintroductions


Biodiversity of man-made open habitats in an underused country: a class of multispecies abundance models for count data by Yuichi Yamaura; J. Andrew Royle; Naoaki Shimada; Seigo Asanuma; Tamotsu Sato; Hisatomo Taki; Shun’ichi Makino (pp. 1365-1380).
Since the 1960s, Japan has become highly dependent on foreign countries for natural resources, and the amount of managed lands (e.g. coppice, grassland, and agricultural field) has declined. Due to infrequent natural and human disturbance, early-successional species are now declining in Japan. Here we surveyed bees, birds, and plants in four human-disturbed open habitats (pasture, meadow, young planted forest, and abandoned clear-cut) and two forest habitats (mature planted forest and natural old-growth). We extended a recently developed multispecies abundance model to accommodate count data, and used the resulting models to estimate species-, functional group-, and community-level state variables (abundance and species richness) at each site, and compared them among the six habitats. Estimated individual-level detection probability was quite low for bee species (mean across species = 0.003; 0.16 for birds). Thirty-two (95% credible interval: 13–64) and one (0–4) bee and bird species, respectively, were suggested to be undetected by the field survey. Although habitats in which community-level abundance and species richness was highest differed among taxa, species richness and abundance of early-successional species were similar in the four disturbed open habitats across taxa except for plants in the pasture habitat which was a good habitat only for several exotic species. Our results suggest that human disturbance, especially the revival of plantation forestry, may contribute to the restoration of early-successional species in Japan.

Keywords: Count data; Functional group; Hierarchical community model; Human disturbance; Plantation forestry; Species richness


Phyllostomid bat assemblages in different successional stages of tropical rain forest in Chiapas, Mexico by Erika de la Peña-Cuéllar; Kathryn E. Stoner; Luis Daniel Avila-Cabadilla; Miguel Martínez-Ramos; Alejando Estrada (pp. 1381-1397).
Due to their role in seed dispersal, changes in the community of phyllostomid bats have direct consequences on ecological succession. The objective of this work was to document changes in the structure of bat assemblages among secondary successional stages of tropical rain forest in Chiapas, Mexico. Bats were mist-netted at ground level during 18 months in 10 sites belonging to 3 successional stages: four sites represented early succession (2–8 years of abandonment), four intermediate succession (10–20 years of abandonment), and two late succession (mature old-growth forest).We captured 1,179 phyllostomids comprising 29 species. Phyllostomid species richness was 17 (58% of all species) in the early stage, 18 (62%) in the intermediate stage and 24 (83%) in the late stage. The late successional mature forest possessed nine species that were exclusively found there, whereas early and intermediate successional stages contained only one exclusive species. Sturnira lilium, Artibeus lituratus, Carollia perpicillata, Artibeus jamaicensis and Glossophaga soricina represented 88% of all captured phyllostomid bats. Frugivores made up more than 90% of the species captured in early and intermediate successional stages and 84% in late successional forest. The Bray–Curtis index of dissimilarity showed a replacement of species through successional stages with the largest dissimilarity between early and late stages, followed by intermediate and late, and the lowest dissimilarity between early and intermediate stages. The number of gleaning insectivore species increased during succession. The carnivorous guild was exclusively found in the late stage (three species). We conclude that the late successional mature forest was the main reservoir for the gleaning insectivore and carnivore guilds; however, early and intermediate successional stages possessed a great diversity of species including many frugivores.

Keywords: Species richness; Community structure; Diversity; Frugivores; Guilds; Phyllostomid bats; Succession


Distinguishing between turnover and nestedness in the quantification of biotic homogenization by Lander Baeten; Pieter Vangansbeke; Martin Hermy; George Peterken; Kathleen Vanhuyse; Kris Verheyen (pp. 1399-1409).
Compositional changes through local extinction and colonization are inherent to natural communities, but human activities are increasingly influencing the rate and nature of the species being lost and gained. Biotic homogenization refers to the process by which the compositional similarity of communities increases over time through a non-random reshuffling of species. Despite the extensive conceptual development of the homogenization framework, approaches to quantify patterns of homogenization are scarcely developed. Most studies have used classical dissimilarity indices that actually quantify two components of compositional variation: turnover and nestedness. Here we demonstrate that a method that partitions those two components reveals patterns of homogenization that are otherwise obscured using traditional techniques. The forest understorey vegetation of an unmanaged reserve was recorded in permanent plots in 1979 and 2009. In only thirty years, the local species richness significantly decreased and the variation in the species composition from site to site shifted towards a structure with reduced true species turnover and increased dissimilarity due to nestedness. A classic analysis masked those patterns. In summary, we illustrated the need to move beyond the simple quantification of homogenization using classical indices and advocate integration of the multitude of ways to quantify community similarity into the homogenization framework.

Keywords: Vegetation resurvey; Permanent plot; Forest understorey; Beta diversity; Global changes; Succession


Dependence of anuran diversity on environmental descriptors in farmland ponds by Fernando Rodrigues da Silva; Carolina Panin Candeira; Denise de Cerqueira Rossa-Feres (pp. 1411-1424).
In the Neotropics, conversion of natural habitats into agricultural areas is occurring at a high rate, with consequent reduction of habitat complexity in anuran breeding ponds. Identifying features of farmland ponds that allow them to support a high diversity of species is fundamental for successful management and conservation policies and is especially important in Neotropical regions that harbor the highest anuran species richness in the world. Here, we aimed to investigate which environmental descriptors correlate the occurrence of anuran species in tropical farmland ponds in southeastern Brazil. We found that environmental descriptors reflecting the complexity of vegetation in farmland ponds primarily predict the diversity of anuran species in these habitats. Species richness was correlated mainly by vegetation height in the margin, with ponds that exhibit greater stratification harboring a larger number of species. Vegetation height in the interior of ponds, diversity of vegetation in the margin, pond area and hydroperiod were also important variables predicting the abundance of six of 10 anuran species analyzed. Our results show that features of farmland ponds representing increased habitat complexity are key factors in maintaining a high diversity of species, providing a greater variety of microhabitats, both in vertical and horizontal strata, and thus meeting diverse species-specific requirements.

Keywords: Amphibian; Generalized linear models; Hierarchical partition; Heterogeneity; Mesophytic semideciduous forest


The rarity and overexploitation paradox: stag beetle collections in Japan by Pierline Tournant; Liana Joseph; Koichi Goka; Franck Courchamp (pp. 1425-1440).
For some wildlife commodities, rare species are especially sought after. The tendency for rare commodities to be of higher value can fuel their exploitation and as numbers dwindle, the demand can increase. Consequently, this can precipitate these rare species into an overexploitation vortex where they become increasingly rare, valued and exploited until eventual extinction. We focus here on the hobby of collecting stag beetles, to ascertain if the market value of these items is driven by rarity and if, consequently, these species are vulnerable to this overexploitation vortex. Stag beetle collections fuel a large and lucrative market in Japan, involving more than 700 species from all over the world, with over 15 million specimens imported a year. Some particularly valued species fetch more than US$5,000 a piece. We assessed the importance of species rarity as an acquisition criterion in this market using two methods: an Internet online questionnaire responded to by 509 participants and through examining the quantities imported in Japan and prices paid by collectors. We discovered that species rarity is one of the main choice criteria for acquisition by collectors: rare stag beetles are valued more than the common species and, consequently, stag beetles are vulnerable to the anthropogenic Allee effect in this market. Because of the sheer size of the market and the pervasive nature of this rarity paradox, the attraction to rarity equates to a potential extinction threat for many rare stag beetles species.

Keywords: Anthropogenic Allee effect; Market price; Questionnaire; Extinction risk; Wildlife trade; Collector


Can bison play a role in conserving habitat for endangered sandhills species in Canada? by Thomas A. Fox; Chris H. Hugenholtz; Darren Bender; Cormack C. Gates (pp. 1441-1455).
Relative to their cultivated surroundings, sandhills of the Canadian prairies represent intact, heterogeneous ecosystems. These extensive tracts of sand dunes and native prairie are biodiversity hotspots, which act as refugia for a variety of specialized wildlife species. However, due to changes in climate and suppression of natural disturbance, the dunes have experienced drastic rates of stabilization over the past 200 years, such that the proportion of open sand in the region is currently less than 1%. This continuing trend is resulting in a gradual loss of sparsely vegetated, sandy habitat for many uncommon, specialist species, including a number that are considered to be at risk of extirpation or extinction by COSEWIC (Canada’s list agency). Without management to conserve active sandhill habitat the future long-term survival of rare and imperilled dune-dependent plants and animals is questionable. In this article we propose that the re-introduction of disturbance to southern Canadian prairie sandhills, specifically sandhill use by bison, might be effective in restoring and sustaining actively-eroding sandhill habitat to support some threatened and endangered species. We outline several lines of evidence (geological, geomorphological, archaeological, and historical accounts) indicating bison occupied sandhills and actively modified these ecosystems until European settlement of the prairies. We argue that bison were attracted to sandhills for a number of reasons, and that in great numbers they had considerable influence on sandhills ecosystem functions. Behaviours such as grazing, trailing, wallowing, horning, and trampling created a patchwork mosaic of disturbance effects. We hypothesize that it may be beneficial to reintroduce bison to sandhills ecosystems in the Canadian prairies to restore biodiversity at all levels.

Keywords: Bison; Conservation; Disturbance; Endangered species; Sandhill ecosystems


Selecting flagships for invertebrate conservation by Maan Barua; Daniel J. Gurdak; Riyaz Akhtar Ahmed; Jatin Tamuly (pp. 1457-1476).
Invertebrates have a low public profile and are seriously underrepresented in global conservation efforts. The promotion of flagship species is one way to generate interest in invertebrate conservation. Butterflies are frequently labeled invertebrate flagships, but clear definitions of the conservation actions they are meant to catalyze, and empirical assessments of their popularity amongst non-Western audiences are lacking. To improve the use of invertebrate flagships, we examine how butterflies compare with other taxa in terms of popularity. We then identify characteristics of individual species that are appealing and explore whether these may be used to derive a set of guidelines for selecting invertebrate flagships. We conducted questionnaire-based surveys amongst two target audiences: rural residents (n = 255) and tourists (n = 105) in northeast India. Invertebrates that were aesthetically appealing, or those that provided material benefits or ecological services were liked. Butterflies were the most popular group for both audiences, followed by dragonflies, honeybees and earthworms. A combination of large size and bright colours led to high popularity of individual species, whilst butterflies with unique features were liked by tourists but not rural residents. These results provide empirical evidence that butterflies appeal to diverse audiences and have the potential to be deployed as flagships in different contexts. However, prior to promoting invertebrate flagships, their intended uses need to be specified. Here we define an invertebrate flagship as an invertebrate species or group that resonates with a target audience and stimulates awareness, funding, research and policy support for the conservation of invertebrate diversity. In conclusion we outline a set of heuristic guidelines for selecting flagships to raise awareness of invertebrate diversity and conservation.

Keywords: Biodiversity; Butterflies; Conservation; Flagship species; Insects; Invertebrates; Public perceptions


Effects of agri-environment management for cirl buntings on other biodiversity by Michael A. MacDonald; Gail Cobbold; Fiona Mathews; Matthew J. H. Denny; Leila K. Walker; Philip V. Grice; Guy Q. A. Anderson (pp. 1477-1492).
Agri-environment scheme (AES) management has increased populations of cirl buntings (Emberiza cirlus) in South Devon, England, and might be expected to provide benefits for other declining biodiversity, due to less intensive farm management. Fields managed under AES for cirl buntings (low-input spring barley or permanent pasture without inputs) were contrasted with control fields under conventional management (spring barley without management restrictions and winter cereals, or grazed without management restrictions) to identify such benefits for vascular plants, butterflies, bumblebees, carabid beetles, foliar invertebrates and bats. Activity-density and species richness of carabid beetles were both higher in AES spring barley fields than in control spring barley and winter cereal fields. Forb cover and abundance of butterflies and bumblebees were higher in AES spring barley fields than in winter cereals, but did not differ between AES and control spring barley. No difference was observed in plant species richness between any of the arable field types. Plant species richness and butterfly abundance were higher in AES pasture fields than in controls. Abundance, activity-density and/or species richness of other taxa did not differ between AES and control pastures. Benefits observed in AES spring barley fields arise from management specific to AES agreements, and also, we suggest, from the maintenance of spring-sown barley in the landscape. Benefits in AES pasture fields are ascribed to the absence of fertiliser and pesticide inputs, and reductions in stocking arising from this; there is also likely to have been some pre-selection for older pastures to be entered into AES management agreements. Agri-environment measures for cirl buntings have benefits for a range of taxa beyond the target species, and therefore, largely through reduction of management intensity and maintenance of land-use diversity, improve the overall biodiversity of the farmed landscape where they are present.

Keywords: Agri-environment scheme; Bats; Bumblebees; Butterflies; Carabid beetles; Cirl bunting; Plant species richness reduced input farming; Spring barley


Cross-taxon congruence of α and β diversity among five leaf litter arthropod groups in Colombia by Jimmy Cabra-García; Christian Bermúdez-Rivas; Ana Milena Osorio; Patricia Chacón (pp. 1493-1508).
In this study α and β diversity patterns of five leaf litter arthropod groups (ants, predatory ants, oribatid mites, spiders and other arachnids) were described and compared in 39 sampling patches of a transformed landscape in southwestern Colombia, that represented five vegetation types: secondary forest, riparian forest, giant bamboo forest, pasture and sugarcane crop. It was also assessed whether some taxa could be used as diversity surrogates. A total of 6,765 individuals grouped in 290 morphospecies were collected. Species richness in all groups was lower in highly transformed vegetation types (pasture, sugarcane crop) than in native ones (forests). In contrast, there were no clear tendencies of β diversity among vegetation types. Considering sampling patches, 0.1–42% of the variation in α diversity of one taxonomic group could be explained from the α diversity of another, and 0.2–33% of the variation of β diversity of a given taxon was explained by that in other groups. Contrary to recent findings, we concluded that patterns of α diversity are more congruent than patterns of β diversity. This fact could be attributed to a sampling effect that promotes congruence in α diversity and to a lack of a clear regional ecological gradient that could promote congruent patterns of β diversity. We did not find evidence for an ideal diversity surrogate although diversity patterns of predatory ants had the greatest congruencies. These results support earlier multi-taxon evaluations in that conservation planning should not be based on only one leaf litter arthropod group.

Keywords: Ants; Arachnids; Cross-taxon congruence; Diversity indicators; Multi-taxa inventories; Southwestern Colombia; Surrogate taxa; Tropical dry forest


Comparative changes in density and demography of large herbivores in the Masai Mara Reserve and its surrounding human-dominated pastoral ranches in Kenya by Nina Bhola; Joseph O. Ogutu; Hans-Peter Piepho; Mohamed Y. Said; Robin S. Reid; N. Thompson Hobbs; Han Olff (pp. 1509-1530).
Wildlife habitats in pastoral lands adjoining protected areas in east African savannas are getting progressively degraded, fragmented and compressed by expanding human populations and intensification of land use. To understand the consequences of these influences on wildlife populations, we contrasted the density and demography of 13 wild and three domestic large herbivores between the Masai Mara National Reserve and the adjoining pastoral ranches using aerial surveys conducted in the wet and dry seasons during 1977–2010. Species of different body sizes and feeding styles had different densities between landscapes and seasons. Small-sized herbivores, requiring short, nutritious grasses, and browsers were more abundant in the ranches than the reserve in both seasons. Medium-sized herbivores moved seasonally between landscapes. Larger-bodied herbivores, requiring bulk forage but less susceptible to predation, were more abundant in the reserve than the ranches. The proportions of newborn warthog (Phacochoerus africanus) and juvenile topi (Damaliscus korrigum) were higher in the ranches, with shorter grasses and lower predation risk than in the reserve. These results suggest that pastoral lands adjoining protected areas in African savannas are important as seasonal dispersal and breeding grounds for wild herbivores. However, human population growth and dramatic land use changes are progressively degrading wildlife habitats in pastoral areas, thus restricting the seasonal wildlife dispersal movements between the protected areas and adjoining pastoral lands. Conservation efforts should focus on (1) creating and maintaining functional heterogeneity in protected areas that mimic moderate pastoral grazing conditions to attract small and medium-bodied grazers and (2) securing dispersal areas, including corridors, to ensure continued seasonal large herbivore movements between protected and pastoral systems.

Keywords: Large herbivores; Pastoralism; Protection; Distribution; Seasonal movements


The amphibians of the relict Betampona low-elevation rainforest, eastern Madagascar: an application of the integrative taxonomy approach to biodiversity assessments by Gonçalo M. Rosa; Franco Andreone; Angelica Crottini; J. Susanne Hauswaldt; Jean Noël; Nirhy H. Rabibisoa; Miora O. Randriambahiniarime; Rui Rebelo; Christopher J. Raxworthy (pp. 1531-1559).
The Strict Nature Reserve of Betampona protects one of the last remaining relicts (about 2,228 ha) of low elevation rainforests in eastern Madagascar. Yet little has been previously published about the amphibian fauna of this rainforest. During 2004 and 2007, Betampona was surveyed over a total period of 102 days. Frogs were searched by opportunistic searching, pitfall trapping and acoustic surveys. The survey work confirmed the occurrence of 76 taxa, of which 36 are currently candidate species and about 30% were first considered as undescribed species. The identification of species included a multidimensional and integrative approach that links morphology, bioacoustics, ecology and genetics. Of these taxa, 24 species are potentially endemic to this low elevation eastern region. Considering the relatively small area of the Betampona forest, and its narrow elevational range, 76 amphibian species represents an unusually high richness compared to other sites in Madagascar. Although the eastern region is now largely deforested, our results reveal the importance of this relict forest, which is protecting a diverse amphibian fauna that includes many potentially endemic species.

Keywords: Amphibian conservation; Bioacoustics; DNA barcoding; Batrachofauna; Primary rainforest; Species richness


Assessing the quality and usefulness of different taxonomic groups inventories in a semiarid Mediterranean region by Daniel Bruno; David Sánchez-Fernández; Andrés Millán; Rosa M. Ros; Pedro Sánchez-Gómez; Josefa Velasco (pp. 1561-1575).
Extensive biological databases are valuables ecological research tools that form the basis of biodiversity studies. However, it is essential to perform an assessment of the inventories’ completeness for their use in ecological and conservational research, and this is especially true for non-emblematic groups. Using four exhaustive databases compiled for four taxonomic groups (aquatic beetles, aquatic bugs, bryophytes and orchids), in a semiarid Mediterranean region, the aim of this study was to estimate the degree of completeness for the inventory of each taxa and to identify those spatial units that could be considered to be sufficiently-surveyed (UTM 10 × 10 km squares). Then, the degree of environmental representativeness of the databases was assessed, as well as those factors that could have caused biased sampling efforts. Lastly, the usefulness of each database for conservational purposes was discussed. The results of the present study highlighted the lack of complete and extensive inventory data; as the best sampled group did not even reach 25% of sufficiently-surveyed squares in the territory (in the case of aquatic bugs) and none of the squares presented reliable inventories in the case of bryophytes. Although these results suggested that recording was skewed by relatively simple climatic variables, the sufficiently-surveyed squares were evenly distributed across physioclimatic subregions, what enables their use in further ecological studies. The authors would like to emphasise the potential of these procedures to locate areas in need of further sampling as well as to aid in the design of more effective regional conservation schemes.

Keywords: Aquatic beetles; Aquatic bugs; Biological databases; Bryophytes; Cross-taxon congruence; Environmental representativeness; Orchids; Sampling bias; Species richness; Survey effort


Diversity partitioning of moorland plant communities across hierarchical spatial scales by Takehiro Sasaki; Masatoshi Katabuchi; Chiho Kamiyama; Masaya Shimazaki; Tohru Nakashizuka; Kouki Hikosaka (pp. 1577-1588).
Understanding of the scaling of diversity is critical to enhance conservation strategies for subalpine moorland ecosystems vulnerable to future environmental changes. However, a paucity of quantitative data strongly limits such attempts. In this study, we used an additive diversity partitioning framework and quantified diversity patterns of moorland plant communities across hierarchical spatial scales, within- and between-sample transects, and between sites (corresponding to α and two levels of β diversity). Moorland sites markedly differed in size (range 1,000–160,000 m2) and were isolated from each other to varying extents within an inhospitable matrix (i.e., forests). We found that β diversity components were consistently higher, whereas the local α diversity component was consistently lower than expected by chance. We observed substantial contribution at the between-site scale to total species richness. By focusing on diversity patterns of moorland plant communities across multiple hierarchical spatial scales, we could thus identify the scale at which regional diversity is maximized. Our results suggest that protection of as many moorland sites as possible, to ensure beta diversity between sites, will effectively conserve total diversity. The use of additive diversity partitioning is a major step forward in providing strategies for the biological conservation of subalpine moorland ecosystems vulnerable to future environmental changes.

Keywords: Alpha diversity; Beta diversity; Gamma diversity; Nonrandom processes; Species richness


Subpopulation range estimation for conservation planning: a case study of the critically endangered Cross River gorilla by Sarah C. Sawyer (pp. 1589-1606).
Measuring and characterizing the area utilized by a population or species is essential for assessment of conservation status and for effective allocation of habitat to ensure population persistence. Yet population-level range delineation is complicated by the variety of available techniques coupled with a lack of empirical methods to compare the relative value of these techniques. This study assesses the effect of model choice on resulting subpopulation range estimation for the critically endangered and patchily distributed Cross River gorilla, and evaluates the conservation conclusions that can be drawn from each model. Models considered range from basic traditional approaches (e.g. minimum convex polygon) to newer home range techniques such as local convex hull (LoCoH). Overlap analysis comparing sub-sampled to complete data sets are used to evaluate the robustness of various modeling techniques to data limitations. Likelihood cross validation criterion is employed to compare core range model performance. Results suggest that differing LoCoH models produce similar range estimates, are robust to data requirements, provide a good fit for core habitat estimation, and are best able to detect unused habitat within the subpopulation range. LoCoH methods may thus be useful for studies into habitat selection and factors limiting endangered species distributions. However, LoCoH models tend to over-fit data, and kernel methods may provide similar information about animal space use while supporting protection of larger swaths of critical habitat. Subpopulation range analyses for conservation/management planning should therefore explore multiple modeling techniques, and employ both qualitative and quantitative assessments to select the best models to inform decision making for species of conservation concern.

Keywords: Conservation planning; Cross River gorilla; Cross validation criterion; Home range analysis; Local convex hull


Reptile responses to fire and the risk of post-disturbance sampling bias by Don A. Driscoll; Annabel L. Smith; Samantha Blight; John Maindonald (pp. 1607-1625).
Altered fire regimes are a driver of biodiversity decline. To plan effective management, we need to know how species are influenced by fire and to develop theory describing fire responses. Animal responses to fire are usually measured using methods that rely on animal activity, but animal activity may vary with time since fire, potentially biasing results. Using a novel approach for detecting bias in the pit-fall trap method, we found that leaf-litter dependent reptiles were more active up to 6 weeks after fire, giving a misleading impression of abundance. This effect was not discovered when modelling detectability with zero-inflated binomial models. Two species without detection bias showed early-successional responses to time since fire, consistent with a habitat-accommodation succession model. However, a habitat specialist did not have the predicted low abundance after fire due to increased post-fire movement and non-linear recovery of a key habitat component. Interactions between fire and other processes therefore must be better understood to predict reptile responses to changing fire-regimes. We conclude that there is substantial bias when trapping reptiles after fire, with species that are otherwise hard to detect appearing to be abundant. Studies that use a survey method based on animal activity such as bird calls or animal movements, likely face a similar risk of bias when comparing recently-disturbed with control sites.

Keywords: Adaptive management; Biological legacies; Disturbance regime; Keystone species; Prescribed burning; State and transition model

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