Carryover effects from environmental change in early life: An overlooked driver of the amphibian extinction crisis?

Ecological carryover effects, or delayed effects of the environment on an organism's phenotype, are central predictors of individual fitness and a key issue in conservation biology. Climate change imposes increasingly variable environmental conditions that may be challenging to early life-history stages in animals with complex life histories, leading to detrimental physiological and fitness effects in later life. Yet, the latent nature of carryover effects, combined with the long temporal scales over which they can manifest, means that this phenomenon remains understudied and is often overlooked in short-term studies limited to single life-history stages. Herein, we review evidence for the physiological carryover effects induced by elevated ultraviolet radiation (UVR; 280–400 nm) as a potential contributor to recent amphibian population declines. UVR exposure causes a suite of molecular, cellular and physiological consequences known to underpin carryover effects in other taxa, but there is a lack of research linking embryonic and larval UVR exposures to fitness consequences post-metamorphosis in amphibians. We propose that the key impacts of UVR on disease-related amphibian declines are facilitated through carryover effects that bridge embryonic and larval UVR exposure with potential increased disease susceptibility post-metamorphosis. We conclude by identifying a practical direction for the study of ecological carryover effects in amphibians that could guide future ecological research in the broader field of conservation physiology. Only by addressing carryover effects can many of the mechanistic links between environmental change and population declines be elucidated.     

Rapid warming is associated with population decline among terrestrial birds and mammals globally

Animal populations have undergone substantial declines in recent decades. These declines have occurred alongside rapid, human‐driven environmental change, including climate warming. An association between population declines and environmental change is well established, yet there has been relatively little analysis of the importance of the rates of climate warming and its interaction with conversion to anthropogenic land use in causing population declines. Here we present a global assessment of the impact of rapid climate warming and anthropogenic land use conversion on 987 populations of 481 species of terrestrial birds and mammals since 1950. We collated spatially referenced population trends of at least 5 years’ duration from the Living Planet database and used mixed effects models to assess the association of these trends with observed rates of climate warming, rates of conversion to anthropogenic land use, body mass, and protected area coverage. We found that declines in population abundance for both birds and mammals are greater in areas where mean temperature has increased more rapidly, and that this effect is more pronounced for birds. However, we do not find a strong effect of conversion to anthropogenic land use, body mass, or protected area coverage. Our results identify a link between rapid warming and population declines, thus supporting the notion that rapid climate warming is a global threat to biodiversity.     

Six years of wild bee monitoring shows changes in biodiversity within and across years and declines in abundance

Wild bees form diverse communities that pollinate plants in both native and agricultural ecosystems making them both ecologically and economically important. The growing evidence of bee declines has sparked increased interest in monitoring bee community and population dynamics using standardized methods. Here, we studied the dynamics of bee biodiversity within and across years by monitoring wild bees adjacent to four apple orchard locations in Southern Pennsylvania, USA. We collected bees using passive Blue Vane traps continuously from April to October for 6 years (2014–2019) amassing over 26,000 bees representing 144 species. We quantified total abundance, richness, diversity, composition, and phylogenetic structure. There were large seasonal changes in all measures of biodiversity with month explaining an average of 72% of the variation in our models. Changes over time were less dramatic with years explaining an average of 44% of the variation in biodiversity metrics. We found declines in all measures of biodiversity especially in the last 3 years, though additional years of sampling are needed to say if changes over time are part of a larger trend. Analyses of population dynamics over time for the 40 most abundant species indicate that about one third of species showed at least some evidence for declines in abundance. Bee family explained variation in species‐level seasonal patterns but we found no consistent family‐level patterns in declines, though bumble bees and sweat bees were groups that declined the most. Overall, our results show that season‐wide standardized sampling across multiple years can reveal nuanced patterns in bee biodiversity, phenological patterns of bees, and population trends over time of many co‐occurring species. These datasets could be used to quantify the relative effects that different aspects of environmental change have on bee communities and to help identify species of conservation concern.     

Shedding light on moths: shorter wavelengths attract noctuids more than geometrids

With moth declines reported across Europe, and parallel changes in the amount and spectra of street lighting, it is important to understand exactly how artificial lights affect moth populations. We therefore compared the relative attractiveness of shorter wavelength (SW) and longer wavelength (LW) lighting to macromoths. SW light attracted significantly more individuals and species of moth, either when used alone or in competition with LW lighting. We also found striking differences in the relative attractiveness of different wavelengths to different moth groups. SW lighting attracted significantly more Noctuidae than LW, whereas both wavelengths were equally attractive to Geometridae. Understanding the extent to which different groups of moth are attracted to different wavelengths of light will be useful in determining the impact of artificial light on moth populations.     

Impacts of thermal mismatches on chytrid fungus Batrachochytrium dendrobatidis prevalence are moderated by life stage,body size,elevation and latitude

Global climate change is increasing the frequency of unpredictable weather conditions; however, it remains unclear how species‐level and geographic factors, including body size and latitude, moderate impacts of unusually warm or cool temperatures on disease. Because larger and lower‐latitude hosts generally have slower acclimation times than smaller and higher‐latitude hosts, we hypothesised that their disease susceptibility increases under ‘thermal mismatches’ or differences between baseline climate and the temperature during surveying for disease. Here, we examined how thermal mismatches interact with body size, life stage, habitat, latitude, elevation, phylogeny and International Union for Conservation of Nature (IUCN) conservation status to predict infection prevalence of the chytrid fungus Batrachochytrium dendrobatidis (Bd) in a global analysis of 32 291 amphibian hosts. As hypothesised, we found that the susceptibility of larger hosts and hosts from lower latitudes to Bd was influenced by thermal mismatches. Furthermore, hosts of conservation concern were more susceptible than others following thermal mismatches, suggesting that thermal mismatches might have contributed to recent amphibian declines.     

Experimental Infection and Repeat Survey Data Indicate the Amphibian Chytrid Batrachochytrium dendrobatidis May Not Occur on Freshwater Crustaceans in Northern Queensland, Australia

Chytridiomycosis is a fatal disease of amphibians, caused by the amphibian chytrid Batrachochytrium dendrobatidis. The disease is unusual in that it may drive many amphibian species to local extinction during outbreaks. These dramatic declines in host population numbers could be facilitated if the pathogen can grow as a saprobe or on alternative hosts, a feature common to other chytrid species. This is also supported by in vitro work that demonstrates B. dendrobatidis can grow and reproduce in the absence of amphibian cells. In a previous study, B. dendrobatidis was detected on freshwater shrimp from rain forest streams in northern Queensland, Australia, using diagnostic PCR. We set out to confirm and further investigate the presence of B. dendrobatidis on crustaceans by carrying out more extensive sampling of shrimp in the field, experimental B. dendrobatidis infection trials using shrimp and crayfish, and PCR verification of the presence of B. dendrobatidis from shrimp samples that previously tested positive. We could not confirm the presence of B. dendrobatidis on shrimp, and report that original positive tests in shrimp reported by Rowley et al. (2006) were likely false. Thus, we suggest that shrimp may not be an important reservoir host for B. dendrobatidis.     

Significant effects of season and bird age on use of coppice woodland by songbirds

Woodland birds have experienced widespread population declines across Europe, resulting partly from a decrease in management practices such as coppicing. Increasing fuelwood demand may reverse the decline of coppicing, making it timely to attempt a fuller understanding of its effects. Here, the impact of coppicing on year‐round habitat use by adults and juveniles of 16 songbird species was quantified from a quasi‐experimental study over 32 years (1978–2009) in Treswell Wood, Nottinghamshire, UK. Habitat use was inferred using capture rates from more than 10 000 h of mist‐netting (> 25 000 captures) and detailed information on coppicing. Capture rates varied with coppice age in different ways: (1) increases as coppice aged (e.g. Marsh Tit Poecile palustris, juvenile Eurasian Treecreepers Certhia familiaris); (2) declines as coppice aged (e.g. Eurasian Blue Tit Cyanistes caeruleus, Great Tit Parus major); (3) peaks in capture rates at intermediate coppice age (i.e. 5–15 years) (e.g. Garden Warbler Sylvia borin, Willow Warbler Phylloscopus trochilus, adult Treecreepers); and (4) a peak at intermediate ages, followed by a decline, before an increase in use again at the oldest coppice ages (i.e. > 20 years) (e.g. Common Blackbird Turdus merula, Eurasian Blackcap Sylvia atricapilla, Eurasian Bullfinch Pyrrhula pyrrhula). Responses to coppice age were similar in different seasons, although Willow Tits Poecile montana showed little preference during breeding but avoided older coppice at other times. Juveniles and adults often differed in their responses to coppice age. The analyses reveal patterns in habitat use that are relevant to woodland management and conservation policy. They suggest that a mosaic of age structures in woodland is beneficial to a wide range of woodland species, and that management should consider the requirements of all age‐classes of birds at different times of year.     

Carnivores (Mammalia: Carnivora) in South China: a status review with notes on the commercial trade

• 1 Evidence from the literature, interviews, market surveys, general rapid field surveys and camera trapping was reviewed to infer the regional status of 33 recorded carnivores in South China (Guangxi, Guangdong, Hainan, Hong Kong and Macau).
• 2 The carnivore fauna in South China is among the most depleted for any continental area in the world.
• 3 The tiger Panthera tigris, leopard Panthera pardus, grey wolf Canis lupus and binturong Arctictis binturong are probably extirpated.
• 4 The dhole Cuon alpinus, Asiatic golden cat Catopuma temmincki and clouded leopard Neofelis nebulosa are at great risk of regional extirpation, as are the more ecologically adaptable red fox Vulpes vulpes, raccoon dog Nyctereutes procyonoides, Asian badger Meles leucurus, Eurasian otter Lutra lutra, Oriental small‐clawed otter Aonyx cinereus and large Indian civet Viverra zibetha.
• 5 Though more widely reported, the Asiatic black bear Ursus thibetanus, yellow‐throated marten Martes flavigula, hog badger Arctonyx collaris and Siberian weasel Mustela sibirica are at regional risk.
• 6 The status of the Burmese ferret‐badger Melogale personata, stripe‐backed weasel Mustela strigidorsa, smooth‐coated otter Lutrogale perspicillata, large‐spotted civet Viverra megaspila and Owston's palm civet Chrotogale owstoni is uncertain due to inadequate information.
• 7 Five carnivore species – the Chinese ferret‐badger Melogale moschata, masked palm civet Paguma larvata, yellow‐bellied weasel Mustela kathiah, small Indian civet Viverricula indica and leopard cat Prionailurus bengalensis– are relatively secure (though not common) in the region, along with the Asian palm civet Paradoxurus hermaphroditus and the Javan mongoose Herpestes javanicus in some areas, while the spotted linsang Prionodon pardicolor and crab‐eating mongoose Herpestes urva may have been under‐reported.
• 8 The main threats have been habitat destruction and unsustainable exploitation. Only in Hong Kong, where enforcement of protection legislation has been stronger, are the surviving carnivore species easily encountered.
• 9 Improved enforcement and monitoring are essential to retaining the remainder of South China's carnivores. Support could be boosted by conservation education and better research.

     

Do pathogens become more virulent as they spread? Evidence from the amphibian declines in Central America

The virulence of a pathogen can vary strongly through time. While cyclical variation in virulence is regularly observed, directional shifts in virulence are less commonly observed and are typically associated with decreasing virulence of biological control agents through coevolution. It is increasingly appreciated, however, that spatial effects can lead to evolutionary trajectories that differ from standard expectations. One such possibility is that, as a pathogen spreads through a naive host population, its virulence increases on the invasion front. In Central America, there is compelling evidence for the recent spread of pathogenic Batrachochytrium dendrobatidis (Bd) and for its strong impact on amphibian populations. Here, we re-examine data on Bd prevalence and amphibian population decline across 13 sites from southern Mexico through Central America, and show that, in the initial phases of the Bd invasion, amphibian population decline lagged approximately 9 years behind the arrival of the pathogen, but that this lag diminished markedly over time. In total, our analysis suggests an increase in Bd virulence as it spread southwards, a pattern consistent with rapid evolution of increased virulence on Bd''s invading front. The impact of Bd on amphibians might therefore be driven by rapid evolution in addition to more proximate environmental drivers.