Biological survey [letter to the Editor]
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High dispersal in a frog species suggests that it is vulnerable to habitat fragmentation
Global losses of amphibian populations are a major conservation concern and their causes have generated substantial debate. Habitat fragmentation is considered one important cause of amphibian decline. However, if fragmentation is to be invoked as a mechanism of amphibian decline, it must first be established that dispersal is prevalent among contiguous amphibian populations using formal movement estimators. In contrast, if dispersal is naturally low in amphibians, fragmentation can be disregarded as a cause of amphibian declines and conservation efforts can be focused elsewhere. We examined dispersal rates in Columbia spotted frogs ( Rana luteiventris ) using capture–recapture analysis of over 10 000 frogs in combination with genetic analysis of microsatellite loci in replicate basins. We found that frogs had exceptionally high juvenile dispersal rates (up to 62% annually) over long distances (>5 km), large elevation gains (>750 m) and steep inclines (36° incline over 2 km) that were corroborated by genetic data showing high gene flow. These findings show that dispersal is an important life-history feature of some amphibians and suggest that habitat fragmentation is a serious threat to amphibian persistence.
Montana↗
A trade-off between embryonic development rate and immune function of avian offspring is concealed by embryonic temperature
Long embryonic periods are assumed to reflect slower intrinsic development that are thought to trade off to allow enhanced physiological systems, such as immune function. Yet, the relatively rare studies of this trade-off in avian offspring have not found the expected trade-off. Theory and tests have not taken into account the strong extrinsic effects of temperature on embryonic periods of birds. Here, we show that length of the embryonic period did not explain variation in two measures of immune function when temperature was ignored, based on studies of 34 Passerine species in tropical Venezuela (23 species) and north temperate Arizona (11 species). Variation in immune function was explained when embryonic periods were corrected for average embryonic temperature, in order to better estimate intrinsic rates of development. Immune function of offspring trades off with intrinsic rates of embryonic development once the extrinsic effects of embryonic temperatures are taken into account.
Arizona↗
Plasticity of parental care under the risk of predation: how much should parents reduce care?
Predation can be an important agent of natural selection shaping parental care behaviours, and can also favour behavioural plasticity. Parent birds often decrease the rate that they visit the nest to provision offspring when perceived risk is high. Yet, the plasticity of such responses may differ among species as a function of either their relative risk of predation, or the mean rate of provisioning. Here, we report parental provisioning responses to experimental increases in the perceived risk of predation. We tested responses of 10 species of bird in north temperate Arizona and subtropical Argentina that differed in their ambient risk of predation. All species decreased provisioning rates in response to the nest predator but not to a control. However, provisioning rates decreased more in species that had greater ambient risk of predation on natural nests. These results support theoretical predictions that the extent of plasticity of a trait that is sensitive to nest predation risk should vary among species in accordance with predation risk.
Biology Letters↗
Pathophysiology of white-nose syndrome in bats: A mechanistic model linking wing damage to mortality
White-nose syndrome is devastating North American bat populations but we lack basic information on disease mechanisms. Altered blood physiology owing to epidermal invasion by the fungal pathogen Geomyces destructans ( Gd ) has been hypothesized as a cause of disrupted torpor patterns of affected hibernating bats, leading to mortality. Here, we present data on blood electrolyte concentration, haematology and acid–base balance of hibernating little brown bats, Myotis lucifugus , following experimental inoculation with Gd . Compared with controls, infected bats showed electrolyte depletion (i.e. lower plasma sodium), changes in haematology (i.e. increased haematocrit and decreased glucose) and disrupted acid–base balance (i.e. lower CO 2 partial pressure and bicarbonate). These findings indicate hypotonic dehydration, hypovolaemia and metabolic acidosis. We propose a mechanistic model linking tissue damage to altered homeostasis and morbidity/mortality.
Biology Letters↗
Homing of invasive Burmese pythons in South Florida: evidence for map and compass senses in snakes
Navigational ability is a critical component of an animal's spatial ecology and may influence the invasive potential of species. Burmese pythons ( Python molurus bivittatus ) are apex predators invasive to South Florida. We tracked the movements of 12 adult Burmese pythons in Everglades National Park, six of which were translocated 21–36 km from their capture locations. Translocated snakes oriented movement homeward relative to the capture location, and five of six snakes returned to within 5 km of the original capture location. Translocated snakes moved straighter and faster than control snakes and displayed movement path structure indicative of oriented movement. This study provides evidence that Burmese pythons have navigational map and compass senses and has implications for predictions of spatial spread and impacts as well as our understanding of reptile cognitive abilities.
Florida↗
Topsy-turvy: Turning the counter-current heat exchange of leatherback turtles upside down
Counter-current heat exchangers associated with appendages of endotherms feature bundles of closely applied arteriovenous vessels. The accepted paradigm is that heat from warm arterial blood travelling into the appendage crosses into cool venous blood returning to the body. High core temperature is maintained, but the appendage functions at low temperature. Leatherback turtles have elevated core temperatures in cold seawater and arteriovenous plexuses at the roots of all four limbs. We demonstrate that plexuses of the hindlimbs are situated wholly within the hip musculature, and that, at the distal ends of the plexuses, most blood vessels supply or drain the hip muscles, with little distal vascular supply to, or drainage from the limb blades. Venous blood entering a plexus will therefore be drained from active locomotory muscles that are overlaid by thick blubber when the adults are foraging in cold temperate waters. Plexuses maintain high limb muscle temperature and avoid excessive loss of heat to the core, the reverse of the accepted paradigm. Plexuses protect the core from overheating generated by muscular thermogenesis during nesting.
Biology Letters↗
Arctic sea ice a major determinant in Mandt's black guillemot movement and distribution during non-breeding season
Mandt's black guillemot ( Cepphus grylle mandtii ) is one of the few seabirds associated in all seasons with Arctic sea ice, a habitat that is changing rapidly. Recent decreases in summer ice have reduced breeding success and colony size of this species in Arctic Alaska. Little is known about the species' movements and distribution during the nine month non-breeding period (September–May), when changes in sea ice extent and composition are also occurring and predicted to continue. To examine bird movements and the seasonal role of sea ice to non-breeding Mandt's black guillemots, we deployed and recovered ( n = 45) geolocators on individuals at a breeding colony in Arctic Alaska during 2011–2015. Black guillemots moved north to the marginal ice zone (MIZ) in the Beaufort and Chukchi seas immediately after breeding, moved south to the Bering Sea during freeze-up in December, and wintered in the Bering Sea January–April. Most birds occupied the MIZ in regions averaging 30–60% sea ice concentration, with little seasonal variation. Birds regularly roosted on ice in all seasons averaging 5 h d −1 , primarily at night. By using the MIZ, with its roosting opportunities and associated prey, black guillemots can remain in the Arctic during winter when littoral waters are completely covered by ice.
Biology Letters↗
Timing of ice retreat alters seabird abundances and distributions in the southeast Bering Sea
Timing of spring sea-ice retreat shapes the southeast Bering Sea food web. We compared summer seabird densities and average bathymetry depth distributions between years with early (typically warm) and late (typically cold) ice retreat. Averaged over all seabird species, densities in early-ice-retreat-years were 10.1% (95% CI: 1.1–47.9%) of that in late-ice-retreat-years. In early-ice-retreat-years, surface-foraging species had increased numbers over the middle shelf (50–150 m) and reduced numbers over the shelf slope (200–500 m). Pursuit-diving seabirds showed a less clear trend. Euphausiids and the copepod Calanus marshallae/glacialis were 2.4 and 18.1 times less abundant in early-ice-retreat-years, respectively, whereas age-0 walleye pollock Gadus chalcogrammus near-surface densities were 51× higher in early-ice-retreat-years. Our results suggest a mechanistic understanding of how present and future changes in sea-ice-retreat timing may affect top predators like seabirds in the southeastern Bering Sea.
Alaska↗
Increasing neonicotinoid use and the declining butterfly fauna of lowland California
The butterfly fauna of lowland Northern California has exhibited a marked decline in recent years that previous studies have attributed in part to altered climatic conditions and changes in land use. Here, we ask if a shift in insecticide use towards neonicotinoids is associated with butterfly declines at four sites in the region that have been monitored for four decades. A negative association between butterfly populations and increasing neonicotinoid application is detectable while controlling for land use and other factors, and appears to be more severe for smaller-bodied species. These results suggest that neonicotinoids could influence non-target insect populations occurring in proximity to application locations, and highlights the need for mechanistic work to complement long-term observational data.
California↗
Mitogenomes and relatedness do not predict frequency of tool-use by sea otters
Many ecological aspects of tool-use in sea otters are similar to those in Indo-Pacific bottlenose dolphins. Within an area, most tool-using dolphins share a single mitochondrial haplotype and are more related to each other than to the population as a whole. We asked whether sea otters in California showed similar genetic patterns by sequencing mitogenomes of 43 otters and genotyping 154 otters at 38 microsatellite loci. There were six variable sites in the mitogenome that yielded three haplotypes, one found in only a single individual. The other two haplotypes contained similar percentages (33 and 36%) of frequent tool-users and a variety of diet types. Microsatellite analyses showed that snail specialists, the diet specialist group that most frequently used tools, were no more related to each other than to the population as a whole. The lack of genetic association among tool-using sea otters compared with dolphins may result from the length of time each species has been using tools. Tool-use in dolphins appears to be a relatively recent innovation (less than 200 years) but sea otters have probably been using tools for many thousands or even millions of years.
Biology Letters↗
Insular biogeographic origins and high phylogenetic distinctiveness for a recently depleted lizard fauna from Christmas Island, Australia
Striking faunal turnover across Asia and Australasia, most famously along the eastern edge of the Sunda Shelf or ‘Wallace's Line’, has been a focus of biogeographic research for over 150 years. Here, we investigate the origins of a highly threatened endemic lizard fauna (four species) on Christmas Island. Despite occurring less 350 km south of the Sunda Shelf, this fauna mostly comprises species from clades centred on the more distant regions of Wallacea, the Pacific and Australia (more than 1000 km east). The three most divergent lineages show Miocene (approx. 23–5 Ma) divergences from sampled relatives; and have recently become extinct or extinct in the wild, likely owing to the recent introduction of a southeast Asian snake ( Lycodon capucinus ). Insular distributions, deep phylogenetic divergence and recent decline suggest that rather than dispersal ability or recent origins, environmental and biotic barriers have impeded these lineages from diversifying on the continental Sunda Shelf, and thereby, reinforced faunal differentiation across Wallace's Line. Our new phylogenetically informed perspective further highlights the rapid loss of ancient lineages that has occurred on Christmas Island, and underlines how the evolutionary divergence and vulnerability of many island-associated lineages may continue to be underestimated.
Christmas Island↗
Local extinction of the Asian tiger mosquito (Aedes albopictus) following rat eradication on Palmyra Atol
The Asian tiger mosquito, Aedes albopictus, appears to have been extirpated from Palmyra Atoll following rat eradication. Anecdotal biting reports, collection records, and regular captures in black-light traps showed the species was present before rat eradication. Since then, there have been no biting reports and no captures over 2 years of extensive trapping (black-light and scent traps). By contrast, the southern house mosquito, Culex quinquefasciatus, was abundant before and after rat eradication. We hypothesize that mammals were a substantial and preferred blood meal for Aedes , whereas Culex feeds mostly on seabirds. Therefore, after rat eradication, humans and seabirds alone could not support positive population growth or maintenance of Aedes . This seems to be the first documented accidental secondary extinction of a mosquito. Furthermore, it suggests that preferred host abundance can limit mosquito populations, opening new directions for controlling important disease vectors that depend on introduced species like rats.
Biology Letters↗
The interaction of exposure and warming tolerance determines fish species vulnerability to warming stream temperatures
Species vulnerability to climate change involves an interaction between the magnitude of change (exposure) and a species's tolerance to change. We evaluated fish species vulnerability to predicted stream temperature increases by examining warming tolerances across the Wyoming fish assemblage. Warming tolerance combines stream temperature with a thermal tolerance metric to estimate how much warming beyond current conditions a species can withstand. Brown trout, rainbow trout and burbot had the lowest warming tolerances and the highest proportion of currently occupied sites that will become unsuitable under predicted temperature increases. These most vulnerable species were coldwater species, but had neither the lowest thermal tolerances nor would they experience the greatest temperature increases. Our results highlight the importance of considering the interaction of exposure and warming tolerance when predicting climate change vulnerability and demonstrate an approach that can be applied broadly.
Wyoming↗
Carotenoid-based skin ornaments reflect foraging propensity in a seabird, Sula leucogaster
Carotenoid-based ornaments are common signalling features in animals. It has long been proposed that such ornaments communicate information about foraging abilities to potential mates. However, evidence linking foraging with ornamentation is largely missing from unmanipulated, free-ranging populations. To investigate this relationship, we studied a coastal population of brown booby ( Sula leucogaster brewsteri ), a seabird with a carotenoid-based gular skin ornament. δ 13 C values from both feathers and blood plasma were negatively correlated with male gular colour, indicating birds that consumed more pelagic prey in offshore locations had more ornamented skin than those that fed on nearshore, benthic prey. This relationship was supported by our GPS tracking results, which revealed longer, more offshore foraging trips among highly ornamented males. Our data show that brown booby ornaments are honest indicators of foraging propensity; a link consistent with the rarity hypothesis and potentially driven by the concentration of carotenoids found in phytoplankton versus benthic algae. Carotenoid-based ornaments may reflect foraging tendencies in animals such as coastal predators that use food webs with distinct carotenoid profiles.
Biology Letters↗
Wait and snap: eastern snapping turtles (Chelydra serpentina) prey on migratory fish at road-stream crossing culverts
There is growing evidence that culverts at road-stream crossings can increase fish density by reducing stream width and fish movement rates, making these passageways ideal predator ambush locations. In this study, we used a combination of videography and δ 13 C stable isotope analyses to investigate predator–prey interactions at a road-stream crossing culvert. Eastern snapping turtles ( Chelydra serpentina ) were found to regularly reside within the culvert to ambush migratory river herring ( Alosa spp.). Resident fish species displayed avoidance of the snapping turtles, resulting in zero attempted attacks on these fish. In contrast, river herring did not display avoidance and were attacked by a snapping turtle on 79% of approaches with a 15% capture rate. Stable isotope analyses identified an apparent shift in turtle diet to consumption of river herring in turtles from culvert sites that was not observed in individuals from non-culvert sites. These findings suggest that anthropogenic barriers like culverts that are designed to allow passage may create predation opportunities by serving as a bottleneck to resident and migrant fish movement.
Biology Letters↗
Social effects of rabies infection in male vampire bats (Desmodus rotundus)
Rabies virus (RABV) transmitted by the common vampire bat ( Desmodus rotundus ) poses a threat to agricultural development and public health throughout the Neotropics. The ecology and evolution of rabies host-pathogen dynamics are influenced by two infection-induced behavioral changes. RABV-infected hosts often exhibit increased aggression which facilitates transmission, and rabies also leads to reduced activity and paralysis prior to death. Although several studies document rabies-induced behavioral changes in rodents and other dead-end hosts, surprisingly few studies have measured these changes in vampire bats, the key natural reservoir throughout Latin America. Here, we take advantage of an experiment designed to test the safety and efficacy of an oral rabies vaccine in captive male vampire bats to quantify for the first time how rabies affects allogrooming and aggressive behaviors in the vampire bat. Compared to non-rabid vampire bats, rabid individuals reduced their allogrooming prior to death, but we did not detect increases in aggression among bats. To put our results in context, we review what is known and what remains unclear about behavioral changes of rabid vampire bats.
Biology Letters↗
Range-wide salamander densities reveal a key component of terrestrial vertebrate biomass in eastern North American forests
Characterizing the population density of species is a central interest in ecology. Eastern North America is the global hotspot for biodiversity of plethodontid salamanders, an inconspicuous component of terrestrial vertebrate communities, and among the most widespread is the eastern red-backed salamander, Plethodon cinereus . Previous work suggests population densities are high with significant geographic variation, but comparisons among locations are challenged by lack of standardization of methods and failure to accommodate imperfect detection. We present results from a large-scale research network that accounts for detection uncertainty using systematic survey protocols and robust statistical models. We analysed mark–recapture data from 18 study areas across much of the species range. Estimated salamander densities ranged from 1950 to 34 300 salamanders ha −1 , with a median of 9965 salamanders ha −1 . We compared these results to previous estimates for P. cinereus and other abundant terrestrial vertebrates. We demonstrate that overall the biomass of P. cinereus , a secondary consumer, is of similar or greater magnitude to widespread primary consumers such as white-tailed deer ( Odocoileus virginianus ) and Peromyscus mice, and two to three orders of magnitude greater than common secondary consumer species. Our results add empirical evidence that P. cinereus , and amphibians in general, are an outsized component of terrestrial vertebrate communities in temperate ecosystems.
Biology Letters↗