# Zoological Society of London

• London, United Kingdom
Recent publications
Anthropogenic changes to the environment are facilitating the spread of animal pathogens into human populations. A global focus on detecting and containing emerging infectious diseases has deflected from the need for upstream prevention measures to reduce the risk of pathogen emergence. The drivers of infectious disease emergence have predominantly been considered as environmental and conservation issues and not as risks to human health. There is an opportunity for the UK to take a leadership position on this complex issue. This will require the establishment and maintenance of effective governance and policy mandates. Novel ways of policymaking are needed urgently to achieve three key aims: coordination and collaboration across sectors and government departments, the inclusion of diverse expertise, and the prioritisation of measures directed at prevention.
Active and passive restoration are both increasingly considered as options for nature recovery, with potential to help address the current climate and biodiversity crises. So far, however, there is little practical information on how to gauge the benefits and limitations of each approach, in terms of their effects on large-scale ecosystem composition, structure, and functioning. To address this knowledge gap, this study used satellite remote sensing to investigate changes in land cover and primary productivity within the forests of the Făgăraș Mountains in southern Romania, where large-scale restoration and land abandonment have simultaneously taken place across the past two decades. To our knowledge, this study is the first to contrast the impacts of active and passive restoration within a single landscape on components of ecosystem structure and functioning at such temporal and spatial scales. Results show active restoration activities to be very effective at facilitating the recovery of cleared forests in small parts of the landscapes; but they also highlight substantial areas of natural forest expansion following agricultural abandonment, in line with regional trends. Altogether, our approach clearly illustrates how freely available satellite data can (1) provide vital spatially explicit insights about large-scale and long-term transformations in ecosystem composition, structure and functioning; and (2) help contrast the impacts of restoration approaches on vegetation distribution and dynamics, in ways that complement existing ground-based studies.
Maternal strategies reflect the trade-off between offspring needs and maternal ability to invest, a concept described by the evolutionary theory of parent–offspring conflict. In mammals this conflict has often been investigated by studying weaning, the transition from maternal milk consumption to dietary independence. An investigation of individual variation in weaning can provide information on the adaptive significance of maternal strategies in relation to social and biological variables. We analysed stable nitrogen isotopes of hair samples collected from 22 mother–infant dyads in a wild population of chacma baboons, Papio ursinus, in conjunction with behavioural data on suckling, to explore the temporal dynamics of weaning, as well as the extent and determinants of individual variation in these dynamics. The weaning pattern suggested by isotope values and behavioural data were congruent. The difference between infant and mother stable nitrogen isotope values decreased faster with age in infants of low-ranking mothers, which suggests a faster progression towards weaning, perhaps due to subordinate females experiencing lower resource availability and so being less able to bear the costs of lactation over prolonged periods. Additionally, within-infant variation in stable nitrogen isotope values showed an increase with age (which was not detectable between infants), potentially highlighting the nutritional costs that weaning imposes on offspring. Our combination of isotope analysis and behavioural data from a wild population provides insight into the evolution of maternal strategies. In particular, it suggests that the quantity of care a mother can provide is affected by her rank, with subordinate females possibly not able to lactate for as long and perhaps benefiting from weaning earlier.
An unintended consequence of smallpox eradication and ending the smallpox vaccination campaign has been to render the global human population immunologically naïve to orthopoxvirus infection for the first time in history. This has occurred at a time when the majority of people worldwide live in high population densities in cities and when connectivity across the world has never been higher, both of which facilitate the emergence and spread of infectious diseases. It is not surprising, therefore, that novel zoonotic orthopoxvirus infections have been increasing in recent years, or that an international outbreak of human monkeypox disease has occurred. A One Health approach, including consideration of land-use change and the bushmeat and exotic pet trades, is required to prevent opportunities for the emergence of monkeypox, or diseases cause by other orthopoxviruses, and for a rapid and effective response to any outbreaks in order to limit their spread. One Health Impact Statement The current global outbreak of monkeypox is yet another warning for the adoption of a preventative, One Health, approach to minimise the risk of future emergence of known and unknown zoonotic pathogens. This includes the need to consider the roles, and to mitigate the impacts, of land-use change and the bushmeat and exotic pet trades in order to prevent opportunities for the emergence of monkeypox virus, or other orthopoxviruses, and for a rapid and effective response to any outbreaks in order to limit their spread. As of 9 September 2022, there have been 56,098 confirmed cases of monkeypox in people in 96 countries since an initial case was confirmed in the UK on 7 May (CDC, 2022). However, this does not include infections in Central and West Africa where the infection is endemic and where human cases of the disease have been escalating dramatically in recent years following smallpox eradication ( Tasamba, 2022 ). Monkeypox virus (MPV), the causative agent of monkeypox, is an orthopoxvirus (OPV) closely related to smallpox virus. Following a global vaccination campaign, the World Health Assembly confirmed the eradication of smallpox in 1980, after which vaccination against this disease was ended. During the following 40 years, therefore, and for the first time in history, the global human population has become immunologically naïve to OPVs ( Dye and Kraemer, 2022 ). This has created a gaping ecological niche that is open to exploitation by a new OPV. It is perhaps not surprising, therefore, that zoonotic infections with at least two previously unknown OPVs have emerged in recent years: Akhmeta pox and Alaska pox ( Vora et al ., 2015 ; Springer et al ., 2017 ). Monkeypox virus is also a zoonotic OPV and, although recognized for many years as a public health threat in waiting subsequent to the decline of smallpox vaccination ( Heymann et al ., 1998 ), monkeypox has remained a neglected disease ( Di Giulio and Eckburg, 2004 ; Parker et al ., 2007 ), which is only now receiving attention following its spread to high-income countries.
Captive insectivore nutrition is challenging due to the differing nutritional profiles of wild and captive diets and an incomplete understanding of both. Ultraviolet B (UVB)-irradiation has recently been explored as a means of improving prey-insect vitamin D3 and Ca content. Although short-term irradiation has been successful in some species, it has been unsuccessful in black field crickets (Gryllus bimaculatus)—a commonly cultured feeder insect. We exposed crickets to UVB irradiation from hatchling to adult stages and measured the vitamin D3 and mineral contents of crickets by sex. We did not detect vitamin D3 (detection limit 0.5 iU/g) or an effect of UVB irradiation on mineral content under either UV+ or UV− conditions. We identified large differences between sexes in Ca, K, Mg and P (females higher) and Cu, Fe, S and Zn (males higher), likely linked to reproductive investment. The differences do not straddle the minimum recommended concentrations of minerals for vertebrate growth and thus may be most relevant to animal nutrition in contexts of particular sensitivity or need. We demonstrate a UV-linked trade-off in cricket performance between individual cricket size and the numbers of crickets produced and characterise the energy costs associated with UVB provision. Our results do not support the use of UVB lighting for G. bimaculatus to improve nutrition but demonstrate previously unreported differences in the nutritional profiles between sexes in this species.
The shape and intensity of natural selection can vary between years, potentially resulting in a chronic reduction of fitness as individuals need to track a continually changing optimum of fitness (i.e., a “lag load”). In endangered species, often characterized by small population size, the lack of genetic diversity is expected to limit the response to this constant need to adjust to fluctuating selection, increasing the fitness burden and thus the risk of extinction. Here, we use long‐term monitoring data to assess whether the type of selection for a key fitness trait (i.e., lay date) differs between two reintroduced populations of a threatened passerine bird, the hihi (Notiomystis cincta). We apply recent statistical developments to test for the presence or absence of fluctuation in selection in both the Tiritiri Mātangi Island and the Kārori sanctuary populations. Our results support the presence of stabilizing selection in Tiritiri Mātangi with a potential moving optimum for lay date. In Kārori our results favour a regime of directional selection. Although the shape of selection may differ, for both populations an earlier lay date generally increases fitness in both environments. Further, the moving optimum models of lay date on Tiritiri Mātangi, suggesting that selection varies between years, imply a substantial lag load in addition to the fitness burden caused by the population laying too late. Our results highlight the importance of characterizing the form and temporal variation of selection for each population to predict the effects of environmental change and to inform management. Shape and fluctuation of selection on lay date varies between two re‐introduced populations of the threatened hihi in Aotearoa New Zealand, imposing very different constraints and potential burdens for individual fitness.
In 2021, the International Union for Conservation of Nature (IUCN) introduced a novel method for assessing species recovery and conservation impact: the IUCN Green Status of Species. The Green Status standardizes recovery using a metric called the Green Score, which ranges from 0% to 100%. This study focuses on one crucial step in the Green Status method—the division of a species’ range into so-called “spatial units”—and evaluates whether different approaches for delineating spatial units affect the outcome of the assessment (i.e., the Green Score). We compared Green Scores generated using biologically based spatial units (the recommended method) to Green Scores generated using ecologically based or country-based spatial units for 29 species of birds and mammals in Europe. We found that while spatial units delineated using ecoregions and countries (fine-scale) produced greater average numbers of spatial units and significantly lower average Green Scores than biologically based spatial units, coarse-scale spatial units delineated using biomes and countries above a range proportion threshold did not differ significantly from biologically based results for average spatial unit number or average Green Score. However, case studies focusing on results for individual species (rather than a group average) showed that, depending on characteristics of the species’ distribution, even these coarse-scale delineations of ecological or country spatial units often over- or under-predict the Green Score compared to biologically based spatial units. We discuss cases in which the use of ecologically based or country-based spatial units is recommended or discouraged, in hopes that our results will strengthen the new Green Status framework and ensure consistency in application.
The influence of supplementary feeding of wildlife on disease transmission and its consequent impacts on population dynamics are underappreciated. In Great Britain, supplementary feeding is hypothesised to have enabled the spread of the protozoan parasite, Trichomonas gallinae, from columbids to finches, leading to epidemic finch trichomonosis and a rapid population decline of greenfinch (Chloris chloris). More recently, chaffinch (Fringilla coelebs), has also declined markedly from the second to fifth commonest bird in Britain. Using citizen science data, we show that both declines were driven primarily by reduced adult survival, with the greatest reductions occurring in peri-domestic habitats, where supplementary food provision is common. Post-mortem examinations showed a proportional increase in chaffinch trichomonosis cases, near-contemporaneous with its population decline. Like greenfinches, chaffinches often use supplementary food, but are less associated with human habitation. Our results support the hypothesis that supplementary feeding can increase parasite transmission frequency within and between common species. However, the dynamics behind resultant population change can vary markedly, highlighting the need for integrating disease surveillance with demographic monitoring. Other species susceptible to T. gallinae infection may also be at risk. Supplementary feeding guidelines for wildlife should include disease mitigation strategies to ensure that benefits to target species outweigh risks.
Escherichia albertii is a recently identified gastrointestinal bacterial pathogen of humans and animals which is typically misidentified and generally only detected during genomic surveillance of other Enterobacteriaceae. The incidence of E. albertii is likely underestimated and its epidemiology and clinical relevance are poorly characterised. Here, we whole genome sequenced E. albertii isolates from humans ( n = 83) and birds ( n = 79) in Great Britain and analysed a broader public dataset (n = 475) to address these gaps. We found human and avian isolates typically (90%; 148/164) belonged to host-associated monophyletic groups with distinct virulence and antimicrobial resistance profiles. Overlaid patient epidemiological data suggested that human infection was likely related to travel and possibly foodborne transmission. The Shiga toxin encoding stx2f gene was associated with clinical disease (OR = 10.27, 95% CI = 2.98–35.45 p = 0.0002) in finches. Our results suggest that improved future surveillance will further elucidate disease ecology and public and animal health risks associated with E. albertii .
As the top predator in African ecosystems, lions have lost more than 90% of their historical range, and few countries possess strong evidence for stable populations. Translocations (broadly defined here as the capture and movement of lions for various management purposes) have become an increasingly popular action for this species, but the wide array of lion translocation rationales and subsequent conservation challenges stemming from poorly conceived or unsuitable translocations warrants additional standardized evaluation and guidance. At their best, translocations fill a key role in comprehensive strategies aimed at addressing the threats facing lions and fostering the recovery of wild populations in their historic range. At their worst, translocations can distract from addressing the major threats to wild populations and habitats, divert scarce funding from more valuable conservation actions, exacerbate conflict with humans in recipient sites, disrupt local lion demography, and undermine the genetic integrity of wild lion populations in both source and recipient sites. In the interest of developing best practice guidelines for deciding when and how to conduct lion translocations, we discuss factors to consider when determining whether a translocation is of conservation value, introduce a value assessment for translocations, and provide a decision matrix to assist practitioners in improving the positive and reducing the negative outcomes of lion translocation.
threatened with extinction, resulting in a sampled RLI of 0.914 for all species, 0.968 in marine and 0.862 in freshwater ecosystems. Our sample showed fishing as the principal threat for marine species, and pollution by agricultural and forestry effluents for freshwater fishes. The sampled list provides a robust representation for tracking trends in the conservation status of the world's fishes, including disaggregated sampled indices for marine and freshwater fish. Reassessment and backcasting of this index is urgent to check the achievement of the commitments proposed in global biodiversity targets. Abstract Global biodiversitytargets require us to identify species at risk of extinction and quantify status and trends of biodiversity. The Red List Index (RLI) tracks trends in the conservation status of entire species groups over time by monitoring changes in categories assigned to species. Here, we calculate this index for the world's fishes in 2010, using a sampled approach to the RLI based on a randomly selected sample of 1,500 species, and also present RLI splits for freshwater and marine systems separately. We further compare specific traits of a worldwide fish list to our sample to assess its representativeness. Overall, 15.1% of species in the sample were estimated to be
Rhino rays, such as guitarfishes, are increasingly targeted or retained as incidental catch and have become an economically important component in fisheries worldwide. Despite their importance, information about the catch and socioeconomics of these fisheries are virtually non-existent in West Africa. We address a significant knowledge gap about the characteristics and drivers of guitarfish fisheries in four key ray-fishing communities in the Western and Central Regions in Ghana. We conducted landing and market surveys of guitarfishes over 80 days from November 2020 to August 2021. We also interviewed 51 fishers actively involved in the guitarfish fishery across the four communities during this period using semi-structured interviews. The findings confirm the likely disappearance of sawfishes Pristis spp., as most fishers have not captured any in their lifetime. We also confirm no known catches of the African wedgefish Rhynchobatus luebberti. Our surveys documented 537 individuals from four guitarfish species across the various landing and market sites. The spineback guitarfish (Rhinobatos irvinei) was the most frequently landed species comprising 71 % (n = 383) of all guitarfishes, with 57 % of the specimens not yet sexually mature. Most fishers (71 %) stated that catches of the two larger guitarfishes (blackchin guitarfish Glaucostegus cemiculus and common guitarfish Rhinobatos rhinobatos) have declined by 80–90 % based on their recollection. At the same time, over half (59 %) of the fishers indicated that the catches of the smaller guitarfishes (spineback guitarfish and whitespotted guitarfish Rhinobatos albomaculatus) have declined by 40–60 %. The main drivers for the catch or retention of guitarfishes were for both international trade of their fins, and meat which are both traded locally (45 % of 51 fishers) and used as a source of food for local consumption (37 %). While we know high economic value drives the catch and trade of giant guitarfishes and wedgefishes, we show that this trade extends to the other guitarfish species. The interviews and contemporary pattern of catches are consistent with a serial depletion of rhino rays from the largest, most valuable species to the remaining smaller-bodied, less valuable guitarfishes. We recommend the development of national regulations for their protection complemented by education programs to ensure that fishers are aware of the threatened status of guitarfishes.
Species distribution models are valuable tools for conservation management. However, there remain challenges in developing and interpreting these models in the marine environment, such as the nature of the species used for the modelling process. When working with mobile species in dynamic environments, lack of observation is usually interpreted as an observation of absence, which can result in the introduction of biases by methodological (false) absences. Here, we explore the role of absences when modelling marine megafauna distributions. To better understand how the use of absences (or equivalent) affects the niche modelling algorithms, we used a set of 20 virtual species with different relations to the habitat (generalist static, specialist static, generalist dynamic and specialist dynamic) with different encounter rates. We tested six different modelling techniques divided into three distinct groups: presence-only, presence-background and presence-absence. We compared the outputs of the models using traditional validation metrics and overlap metrics in the geographical and environmental spaces. Algorithms characterized the ecological niche for the simulated species differently. Approaches using background data generally outperformed the other methods, suggesting that the non-observation of a species in a given location and time should not be considered as an absence. A very intense (practically unrealistic) sampling schema would be required to obtain a genuine unbiased absence when working with these species and habitats. For highly mobile species, a precautionary approach would be to consider the non-observation of a species as part of the background (a sample of the conditions available in the study area) rather than an absence. A good starting point would be to use presence-background models, complemented with presence-absence and/or presence-only models, comparing outputs from the different algorithms tested in the geographic and environmental space. Improving model performance for highly mobile marine species should lead to better-informed decision making for conservation.
As a key parameter in population genetics, relatedness has found wide applications in molecular ecology, evolutionary biology, conservation, forensics and in studies of human inheritable diseases. It is defined as the probability that two individuals share an allele due to recent common ancestry. Many estimators have been developed to estimate relatedness from genotype data. However, they are invariably biased when a sample is small or contains a high proportion of close relatives, because allele frequencies required for inferring relatedness are poorly estimated in both cases under the impracticable and yet indispensable assumption of a large sample of unrelated genotypes. In this study, I develop a likelihood method to estimate relatedness and allele frequencies jointly from a sample of multilocus genotypes. I propose an expectation maximization (EM) algorithm to update allele frequencies and the nine condensed identical by descent (IBD) coefficients (∆i,i=1,2,…,9$${\Delta }_i,i=1,2,\dots, 9$$) of each pair of sampled individuals iteratively till convergence. Relatedness between and inbreeding coefficients of individuals is then calculated from the estimated nine IBD coefficients. The EM algorithm is also implemented in the reduced non‐inbreeding model (∆i≡0,i=1,2,…,6$${\Delta }_i\equiv 0,i=1,2,\dots, 6$$) to estimate three condensed IBD coefficients (∆i,i=7,8,9$${\Delta }_i,i=7,8,9$$) and relatedness. Using simulated and empirical data, I show that the new method is much less biased and more accurate than previous methods, providing almost unbiased relatedness and inbreeding estimates, when the sampled individuals are few or/and contain many close relatives. The EM algorithm for the likelihood estimator is fast enough to handle a sample with thousands of individuals and millions of markers, thanks to the parallelization using openMP and MPI. The method is implemented in a software package, EMIBD9, that runs on all major computer platforms. This study shows allele frequencies and relatedness, although highly correlated and difficult to disentangle from each other when the only information available is a sample of multilocus genotypes, can be estimated jointly from genotype data of diallelic and multiallelic markers in a likelihood framework. The new method and software are especially useful for analysing small samples (such as ancient samples from museums, or samples from endangered species) and samples with a strong genetic structure.
The level of detail on host communities needed to understand multihost parasite invasions is an unresolved issue in disease ecology. Coarse community metrics that ignore functional differences between hosts, such as host species richness, can be good predictors of invasion outcomes. Yet if host species vary in the extent to which they maintain and transmit infections, then explicitly accounting for those differences may be important. Through controlled mesocosm experiments and modeling, we show that interspecific differences between host species are important for community-wide infection dynamics of the multihost fungal parasite of amphibians (Batrachochytrium dendrobatidis [Bd]), but only up to a point. The most abundant host species in our system, fire salamander larvae (Salamandra salamandra), did not maintain or transmit infections. Rather, two less abundant "auxiliary" host species, Iberian tree frog (Hyla molleri) and spiny toad (Bufo spinosus) larvae, maintained and transmitted Bd. Frogs had the highest mean rates of Bd shedding, giving them the highest contributions to the basic reproduction number, R0. Toad contributions to R0 were substantial, however, and when examining community-level patterns of infection and transmission, the effects of frogs and toads were similar. Specifying more than just host species richness to distinguish salamanders from auxiliary host species was critical for predicting community-level Bd prevalence and transmission. Distinguishing frogs from toads, however, did not improve predictions. These findings demonstrate limitations to the importance of host species identities in multihost infection dynamics. Host species that exhibit different functional traits, such as susceptibility and infectiousness, may play similar epidemiological roles in the broader community.
Mountains are an essential component of the global life-support system. They are characterized by a rugged, heterogenous landscape with rapidly changing environmental conditions providing myriad ecological niches over relatively small spatial scales. Although montane species are well adapted to life at extremes, they are highly vulnerable to human derived ecosystem threats. Here we build on the manifesto ‘World Scientists' Warning to Humanity’, issued by the Alliance of World Scientists, to outline the major threats to mountain ecosystems. We highlight climate change as the greatest threat to mountain ecosystems, which are more impacted than their lowland counterparts. We further discuss the cascade of “knock-on” effects of climate change such as increased UV radiation, altered hydrological cycles, and altered pollution profiles; highlighting the biological and socio-economic consequences. Finally, we present how intensified use of mountains leads to overexploitation and abstraction of water, driving changes in carbon stock, reducing biodiversity, and impacting ecosystem functioning. These perturbations can provide opportunities for invasive species, parasites and pathogens to colonize these fragile habitats, driving further changes and losses of micro- and macro-biodiversity, as well further impacting ecosystem services. Ultimately, imbalances in the normal functioning of mountain ecosystems will lead to changes in vital biological, biochemical, and chemical processes, critically reducing ecosystem health with widespread repercussions for animal and human wellbeing. Developing tools in species/habitat conservation and future restoration is therefore essential if we are to effectively mitigate against the declining health of mountains.
Traditional Chinese Medicine (TCM) is highlighted by conservation practitioners as an ongoing threat to many overharvested plant and animal species, including several charismatic threatened vertebrates. However, studies that provide evidence‐based and practical recommendations on how to better regulate the TCM trade for sustainability and biodiversity conservation remain limited. China is the biggest promotor of and market for TCM and understanding the TCM trade in China is important for global biodiversity conservation. In particular, conservation researchers need to better understand how the TCM trade and its regulations interact with China’s development needs, and should collaborate with TCM communities to propose locally‐adapted suggestions to decision‐makers. However, progress in these areas has been restricted by language, cultural, and knowledge barriers. In this paper, we provide an overview of the current status of TCM‐related regulations in China, identify weaknesses in regulation frameworks, and highlight issues that currently limit our understanding of the magnitude, dynamics, and impact of the trade. We propose changes in trade regulations, actions to enhance law enforcement, and future research directions to encourage a more sustainable TCM trade that benefits both global biodiversity conservation and TCM development.
The Caucasian grouse Lyrurus mlokosiewiczi, one of the most poorly known species of grouse, is experiencing population declines associated with multiple threats. Evaluating species' population status in relation to different local human activities is important to inform conservation and identify suitable management methods, but determining status and threats for poorly known taxa may require assessment of non‐standard sources of ecological information. We investigated what novel insights can be provided by local ecological knowledge (LEK) about population status and threats to the Caucasian grouse, in relation to the comparative status of other co‐occurring wildlife and to different local land‐use activities, and how data on local awareness and attitudes can guide conservation planning for this species. We conducted an interview survey in rural communities in the Arasbaran Biosphere Reserve (ABR), Iran, and collected LEK from 95 respondents within villages situated close to the locations of surviving and extirpated grouse populations. LEK is a useful tool for assessing the status of grouse populations: 41.1% of respondents recognized grouse and 30.5% had seen the species, and respondents within villages situated close to surviving grouse populations had greater awareness, sighting likelihood, and more recent sightings. More respondents considered that grouse and other galliforms had declined in comparison to other wildlife. Decline and disappearance of grouse populations is associated with alteration and disturbance of grouse habitat, with potential drivers including increased cattle grazing and local bans on harvesting fodder. These findings provide a new baseline to guide the development of suitable grassland management strategies (e.g. grazing regimes) for this species, and highlight the importance of further assessment of the effects of habitat disturbance on grouse survival, including understanding local histories of human–environmental interaction. Current landscape management methods are not supported by local people within the ABR, with most respondents disagreeing with the strict conservation measures currently in place, and we recommend that a new management system should be developed for Caucasian grouse conservation, including targeted conservation education and involving local community participation and co‐management. Read the free Plain Language Summary for this article on the Journal blog. Read the free Plain Language Summary for this article on the Journal blog.
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