Culturing freshwater pearl mussel Margaritifera margaritifera: a breakthrough in the conservation of an endangered species.

1. The freshwater pearl mussel Margaritifera margaritifera L. is globally endangered and is threatened by commercial exploitation, pollution and habitat loss throughout its range. Captive breeding would be a valuable tool in enhancing the status of M. margaritifera in the UK. 2. We have developed a semi-natural system for successfully infecting juvenile brown trout with glochidial M. margaritifera, and culturing juvenile mussels in experimental tanks where glochidial M. margaritifera can excyst from fish gills and settle into sediment. 3. Infected fish had less than 1% mortality. Levels of infection varied among fish. Two yearly cohorts of juvenile M. margaritifera were identified from samples of sediment taken from each experimental tank. Individuals range in size from 1.4 mm (2000 cohort) to >3 mm in length (1999 cohort). 4. The number of juvenile M. margaritifera present in the two experimental tanks are estimated to be between 3600 (tank A) and 0 (tank B) for the putative 1999 cohort and between 6000 (tank A) and 13 000 (tank B) for the putative 2000 cohort. 5. This pioneering method for large-scale cultivation of juvenile M. margaritifera is intermediate between the release of infected fish into rivers and the intensive cultivation systems developed in continental Europe and the USA for other species of unionid. This is the first time that large numbers of M. margaritifera have been cultured and represents a significant breakthrough in the conservation of this globally endangered Red Data List species. The method is straightforward and is most cost-effective when undertaken alongside established hatchery processes.

Pollinators of an endemic and endangered species, Mammillaria gaumeri (Cactaceae), in its natural habitat (coastal dune) and in a botanical garden.

Mammillaria gaumeri (Britton & Ross) Orcutt (Cactaceae), an endemic plant of the Yucatan Peninsula, is included by the Mexican government in the list of species that require special protection. Its natural habitat is now restricted to fragmented areas and protection programs involve botanical gardens in growing individuals rescued from disturbed areas. Little information is available on the reproductive characteristics of this species and nothing is known of its pollinators. We investigated the visitors of M. gaumeri flowers, collecting and observing bee species in its natural habitat (i.e., coastal dune) and in a botanical garden, where coastal dune vegetation had been created. Observations were made on plants whose density was artificially increased by grouping flowering individuals. At each site, we: 1) collected insects visiting the flowers; 2) recorded number of visits; and 3) video-recorded bee movements on the flowers. As expected, the number of bee species and visitation frequency were higher at the botanical garden than at the coastal dune. After landing on a flower, bees either inspected the anthers or dived among them. These behaviors, carried out by all observed species, seemed related to the state of the anthers (full or empty of pollen) and stigma lobes (opened or closed). Specifically, visits lasted longer when anthers were full of pollen and stigma lobes were opened. The same bee species recorded on the dune were also recorded at the botanical garden, suggesting that the artificial dune at the botanical garden offered suitable conditions for the natural pollinators of this endangered cactus.

Applying species distribution modelling to identify areas of high conservation value for endangered species: A case study using Margaritifera margaritifera (L.)

The development and implementation of a population supplementation and restoration plan for any endangered species should involve an understanding of the species’ habitat requirements prior to the release of any captive bred individuals. The freshwater pearl mussel, Margaritifera margaritifera, has undergone dramatic declines over the last century and is now globally endangered. In Northern Ireland, the release of captive bred individuals is being used to support wild populations and repatriate the species in areas where it once existed. We employed a combination of maximum entropy modelling (MAXENT) and Generalized Linear Mixed Models (GLMM) to identify ecological parameters necessary to support wild populations using GIS-based landscape scale and ground-truthed habitat scale environmental parameters. The GIS-based landscape scale model suggested that mussel occurrence was associated with altitude and soil characteristics including the carbon, clay, sand, and silt content. Notably, mussels were associated with a relatively narrow band of variance indicating that M. margaritifera has a highly specific landscape niche. The ground-truthed habitat scale model suggested that mussel occurrence was associated with stable consolidated substrates, the extent of bankside trees, presence of indicative macrophyte species and fast flowing water. We propose a three phase conservation strategy for M. margaritifera identifying suitable areas within rivers that (i) have a high conservation value yet needing habitat restoration at a local level, (ii) sites for population supplementation of existing populations and (iii) sites for species reintroduction to rivers where the mussel historically occurred but is now locally extinct. A combined analytical approach including GIS-based landscape scale and ground-truthed habitat scale models provides a robust method by which suitable release sites can be identified for the population supplementation and restoration of an endangered species. Our results will be highly influential in the future management of M. margaritifera in Northern Ireland.

Modelling distributional trends to inform conservation strategies for endangered species

Aim: Species loss has increased significantly over the last 1000 years and is ultimately attributed to the direct and indirect consequences of increased human population growth across the planet. A growing number of species are becoming endangered and require human intervention to prevent their local extirpation or complete extinction. Management strategies aimed at mitigating a species loss can benefit greatly from empirical approaches that indicate the rate of decline of a species providing objective information on the need for immediate conservation actions, e.g. captive breeding; however, this is rarely employed. The current study used a novel method to examine the distributional trends of a model endangered species, the freshwater pearl mussel, Margaritifera margaritifera (L.).
Location: United Kingdom and Republic of Ireland.
Methods: Using species presence data within 10-km grid squares since records began three-parameter logistic regression curves were fitted to extrapolate an estimated date of regional extinction.
Results: This study has shown that freshwater pearl mussel distribution has contracted since known historical records and outlier populations were lost first. Within the United Kingdom and Republic of Ireland, distribution loss has been greatest in Scotland, Northern Ireland, Wales and England, respectively, with the Republic of Ireland containing the highest relative proportion of M. margaritifera distribution, in 1998.
Main conclusions: This study provides empirical evidence that this species could become extinct throughout countries within the United Kingdom within 170 years under the current trends and emphasizes that regionally specific management strategies need to be implemented to prevent extirpation of this species.

High levels of genetic structuring as a result of population fragmentation in the tropical tree species Caesalpinia echinata Lam.

We have investigated levels of genetic diversity within and among seven remnant populations of Caesalpinia echinata Lam., an endangered species found as fragmented populations in three major areas around the coastal regions of Brazil. Using amplified fragment length polymorphism (AFLP) genetic markers, we detected levels of within-population genetic diversity ranging from 0.092 to 0.163, with the lowest values generally being found in the smallest populations. Estimates of between-population genetic differentiation were strongly correlated with geographical distance ( r = 0.884, p <0.001), which, along with a neighbour-joining phylogenetic analysis, strongly suggested high levels of genetic isolation by distance. Over half (62%) of the total genetic diversity was partitioned between populations, further highlighting the genetic distinctness of individual populations. Taken together, these results suggest that fragmentation has led to an increase in population differentiation between fragments of C. echinata. These formations will be of great value in the development of conservation plans for species exhibiting high levels of genetic differentiation due to fragmentation, such as indication of conservation unit size, which populations should be chosen as priority in conservation plans and which samples should be introduced in areas with a low number of individuals of brazilwood.

Indicators of the impact of climate change on migratory species

The Bonn Convention on the Conservation of Migratory Species of Wild Animals adopted a Resolution in 2005 recognising the impacts of climate change on migratory species. It called on Contracting Parties to undertake more research to improve our understanding of these impacts and to implement adaptation measures to reduce foreseeable adverse effects. Given the large diversity of taxa and species affected by climate change, it is impossible to monitor all species and effects thereof. However, it is likely that many of the key ecological and physical processes through which climate change may impact wildlife could be monitored using a suite of indicators, each comprising parameters of species/populations or groups of species as proxies for wider assemblages, habitats and ecosystems. Herein, we identify a suite of 17 indicators whose attributes could reveal negative impacts of climate change on the global status of migratory species: 4 for birds, 4 for marine mammals, 2 for sea turtles, 1 for fish, 3 for land mammals and 3 for bats. A few of these indicators would be relatively straightforward to develop, but most would require additional data collation, and in many cases methodological development. Choosing and developing indicators of the impacts of climate change on migratory species is a challenge, particularly with endangered species, which are subject to many other pressures. To identify and implement conservation measures for these species, indicators must account for the full ensemble of pressures, and link to a system of alerts and triggers for action.

Removing the threat of diclofenac to critically endangered Asian vultures

Veterinary use of the nonsteroidal anti-inflammatory (NSAID) drug diclofenac in South Asia has resulted in the collapse of populations of three vulture species of the genus Gyps to the most severe category of global extinction risk. Vultures are exposed to diclofenac when scavenging on livestock treated with the drug shortly before death. Diclofenac causes kidney damage, increased serum uric acid concentrations, visceral gout, and death. Concern about this issue led the Indian Government to announce its intention to ban the veterinary use of diclofenac by September 2005. Implementation of a ban is still in progress late in 2005, and to facilitate this we sought potential alternative NSAIDs by obtaining information from captive bird collections worldwide. We found that the NSAID meloxicam had been administered to 35 captive Gyps vultures with no apparent ill effects. We then undertook a phased programme of safety testing of meloxicam on the African white-backed vulture Gyps africanus, which we had previously established to be as susceptible to diclofenac poisoning as the endangered Asian Gyps vultures. We estimated the likely maximum level of exposure (MLE) of wild vultures and dosed birds by gavage (oral administration) with increasing quantities of the drug until the likely MLE was exceeded in a sample of 40 G. africanus. Subsequently, six G. africanus were fed tissues from cattle which had been treated with a higher than standard veterinary course of meloxicam prior to death. In the final phase, ten Asian vultures of two of the endangered species (Gyps bengalensis, Gyps indicus) were dosed with meloxicam by gavage; five of them at more than the likely MLE dosage. All meloxicam-treated birds survived all treatments, and none suffered any obvious clinical effects. Serum uric acid concentrations remained within the normal limits throughout, and were significantly lower than those from birds treated with diclofenac in other studies. We conclude that meloxicam is of low toxicity to Gyps vultures and that its use in place of diclofenac would reduce vulture mortality substantially in the Indian subcontinent. Meloxicam is already available for veterinary use in India.

Leatherback turtles satellite-tagged in European waters

The North Atlantic is considered a stronghold for the critically endangered leatherback sea turtle. However, limited information exists regarding the movements of individuals to and from the seas off Europe's northwesterly fringe, an area where featherbacks have been historically sighted for the past 200 yr. Here, we used satellite telemetry to record the movements and behaviour of 2 individuals bycaught in fisheries off the southwest coast of Ireland. The turtle T1 (tagged 1 September 2005; female; tracked 375 d) immediately travelled south via Madeira and the Canaries, before residing in West African waters for 3 mo. In spring, T1 migrated north towards Newfoundland where transmissions ceased. T2 (29 June 2006; male; 233 d) travelled south for a short period before spending 66 d west of the Bay of Biscay, an area previously asserted as a high-use area for leatherbacks. This prolonged high latitude summer residence corresponded with a mesoscale feature evident from satellite imagery, with the implication that this turtle had found a rich feeding site. A marked change in dive behaviour was apparent as the turtle exited this feature and provided useful insights on leatherback diving behaviour. T2 headed south in October 2006, and performed the deepest-ever dive recorded by a reptile (1280 m) southwest of Cape Verde. Unlike T1, T2 swam southwest towards Brazil before approaching the major nesting beaches of French Guiana and Surinam. Importantly, these tracks document the movement of leatherbacks from one of the remotest foraging grounds in the North Atlantic. © Inter-Research 2008.

Prying into the intimate secrets of animal lives; software beyond hardware for comprehensive annotation in 'Daily Diary' tags

BACKGROUND: Smart tags attached to freely-roaming animals recording multiple parameters at infra-second rates are becoming commonplace, and are transforming our understanding of the way wild animals behave. Interpretation of such data is complex and currently limits the ability of biologists to realise the value of their recorded information.

DESCRIPTION: This work presents Framework4, an all-encompassing software suite which operates on smart sensor data to determine the 4 key elements considered pivotal for movement analysis from such tags (Endangered Species Res 4: 123-37, 2008). These are; animal trajectory, behaviour, energy expenditure and quantification of the environment in which the animal moves. The program transforms smart sensor data into dead-reckoned movements, template-matched behaviours, dynamic body acceleration-derived energetics and position-linked environmental data before outputting it all into a single file. Biologists are thus left with a single data set where animal actions and environmental conditions can be linked across time and space.

CONCLUSIONS: Framework4 is a user-friendly software that assists biologists in elucidating 4 key aspects of wild animal ecology using data derived from tags with multiple sensors recording at high rates. Its use should enhance the ability of biologists to derive meaningful data rapidly from complex data.

Four independent gene phylogenies confirm the ancient relationships of Madagascar endemic species in the Papilio demoleus group (Lepidoptera, Papilionidae).

Madagascar is home to numerous endemic species and lineages, but the processes that have contributed to its endangered diversity are still poorly understood. Evidence is accumulating to demonstrate the importance of Tertiary dispersal across varying distances of oceanic barriers, supplementing vicariance relationships dating back to the Cretaceous, but these hypotheses remain tentative in the absence of well-supported phylogenies. In the Papilio demoleus group of swallowtail butterflies, three of the five recognized species are restricted to Madagascar, whereas the remaining two species range across the Afrotropical zone and southern Asia plus Australia. We reconstructed phylogenetic relationships for all species in the P. demoleus group, as well as 11 outgroup Papilio species, using 60 morphological characters and about 4 kb of nucleotide sequences from two mitochondrial (cytochrome oxidase I and II) and two nuclear (wg and EF-1a) genes. Of the three endemic Malagasy species, the two that are formally listed as endangered or at risk represented the most basal divergences in the group, while the more common third endemic was clearly related to African P. demodocus. The fifth species, P. demoleus, showed little differentiation across southern Asia, but showed divergence from its subspecies sthenelus in Australia. Dispersal-vicariance analysis using cladograms derived from morphology and three independent genes indicated a Malagasy diversification of lime swallowtails in the middle Miocene. Thus, diversification processes on the island of Madagascar may have contributed to the origin of common butterflies that now occur throughout much of the Old World tropical and subtemperate regions. An alternative hypothesis, that Madagascar is a refuge for ancient lineages resulting from successive colonizations from Africa, is less parsimonious and does not explain the relatively low continental diversity of the group.

Insights into torpor and behavioural thermoregulation of the endangered Juliana's golden mole

The cryptic, subterranean ways of golden moles (Chrysochloridae) hamper studies of their biology in the field. Ten species appear on the IUCN red list, but the dearth of information available for most inhibits effective conservation planning. New techniques are consequently required to further our understanding and facilitate informed conservation management decisions. We studied the endangered Juliana's golden mole Neamblysomus julianae and aimed to evaluate the feasibility of using implantable temperature sensing transmitters to remotely acquire physiological and behavioural data. We also aimed to assess potential body temperature (T-b) fluctuations in relation to ambient soil temperature (T-a) in order to assess the potential use of torpor. Hourly observations revealed that T-b was remarkably changeable, ranging from 27 to 33 degrees C. In several instances T-b declined during periods of low T-a. Such 'shallow torpor' may result in a daily energy saving of c. 20%. Behavioural thermoregulation was used during periods of high T-a by selecting cooler microclimates, while passive heating was used to raise T-b early morning when T-a was increasing. In contrast to anecdotal reports of nocturnal patterns of activity, our results suggest that activity is flexible, being primarily dependent on T-a. These results exemplify how behavioural patterns and microclimatic conditions can be examined in this and other subterranean mammal species, the results of which can be used in the urgently required conservation planning of endangered Chrysochlorid species.

Conservation status and reproduction of the critically endangered freshwater pearl mussel (Margaritifera margaritifera).

1. Freshwater unionoids are one of the most threatened animal groups worldwide and the freshwater pearl mussel Margaritifera margaritifera is currently listed as critically endangered in Europe. The ‘EC Habitats & Species Directive’ requires that EU member states monitor the distribution and abundance of this species and report regularly on its conservation status.
2. The pearl mussel meta-population in Northern Ireland was surveyed to assess temporal population trends in Special Areas of Conservation (SACs) and mussel reproduction throughout its range.
3. Mussels occurred in six rivers and numbers within three SAC designated sites remained stable between 2004-07 and 2011. The discovery of >8,000 previously unknown individuals in the Owenreagh River contributed to an overall increase (+56.8%) in the total known population. All populations actively reproduced during 2010 with approximately half of all individuals gravid. Moreover, suitable salmonid hosts occurred at all sites with 10.7% of salmon and 22.8% of trout carrying encysted glochidia. Populations were composed entirely of aged individuals with little evidence of recent recruitment.
4. We infer that the break in the life cycle must occur during the juvenile stage when glochidia metamorphose and settle into the interstitial spaces within the substrate. Water quality parameters, most notably levels of suspended solids, exceeded the recommended maximum thresholds in all rivers.
5. We posit that the deposition of silt may be the main cause of juvenile mortality contributing to a lack of recruitment. Consequently, all populations were judged to be in ‘unfavourable’ conservation status. Catchment-level management plans are urgently needed to reduce siltation with the aim of improving recruitment. Our results have implications for the success of ex-situ conservation programmes; specifically, the size at which captive bred juveniles are released into the wild. Further research is required to assess the vulnerabilities of early life stages of M. margaritifera to siltation.