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Response to Lisovski et al.

Lisovski et al. [1] describe the widely recognized limitations of light-level geolocator data for identifying short-distance latitudinal movements, recommend that caution be used when interpreting such data, intimated that we did not use such caution and argued that environmental shading likely explained the Golden-winged Warbler ( Vermivora chrysoptera ) movements described in our 2015 report [2] . Lisovski et al. [1] conclude that the bird movements we reported could not be disentangled from estimation error in stationary animals caused by environmental shading. We argue that, to the contrary, these hypotheses can easily be disentangled because the premise that environmental shading caused synchronous and parallel error among geolocators is false. With their assertion that our location estimates could be biased by >3,500 km on a day with no observable local sources of shading, Lisovski et al. [1] have taken a position of incredulity toward all geolocator-based animal movement data published to date.

Current Biology

Variation in plant defense suppresses herbivore performance

Defensive variability of crops and natural systems can alter herbivore communities and reduce herbivory . However, it is still unknown how defense variability translates into herbivore suppression. Nonlinear averaging and constraints in physiological tracking (also more generally called time-dependent effects) are the two mechanisms by which defense variability might impact herbivores . We conducted a set of experiments manipulating the mean and variability of a plant defense, showing that defense variability does suppress herbivore performance and that it does so through physiological tracking effects that cannot be explained by nonlinear averaging. While nonlinear averaging predicted higher or the same herbivore performance on a variable defense than on an invariable defense, we show that variability actually decreased herbivore performance and population growth rate. Defense variability reduces herbivore performance in a way that is more than the average of its parts. This is consistent with constraints in physiological matching of detoxification systems for herbivores experiencing variable toxin levels in their diet and represents a more generalizable way of understanding the impacts of variability on herbivory . Increasing defense variability in croplands at a scale encountered by individual herbivores can suppress herbivory, even if that is not anticipated by nonlinear averaging.

Current Biology

Climate change: Flowering time may be shifting in surprising ways

Climate change is known to affect regional weather patterns and phenology; however, we lack under-standing of how climate drives phenological change across local spatial gradients. This spatial variation is critical for determining whether subpopulations and metacommunities are changing in unison or diverging in phenology. Divergent responses could reduce synchrony both within species (disrupting gene flow among subpopulations) and among species (disrupting interspecific interactions in communities). We also lack understanding of phenological change in environments where life history events are frequently aseasonal, such as the tropical, arid,and semi-arid ecosystems that cover vast areas.Using a 33-year-long dataset spanning a 1,267-m semi-arid elevational gradient in the southwestern United States, we test whether flowering phenology diverged among subpopulations within species and among five communities comprising 590 species. Applying circular statistics to test for changes in year-round flowering, we show flowering has become earlier for all communities except at the highest elevations. However, flowering times shifted at different rates across elevations likely because of elevation-specific changes in temperature and precipitation, indicating diverging phenologies of neighboring communities. Subpopulations of individual species also diverged at mid-elevation but converged in phenology at high elevation. These changes in flowering phenology among communities and subpopulations are undetectable when data are pooled across the gradient. Furthermore, we show that nonlinear changes in flowering times over the 33-year record are obscured by traditional calculations of long-term trends. These findings reveal greater spatiotemporal complexity in phenological responses than previously recognized and indicate climate is driving phenological reshuffling acrosslocal spatial gradients.

Current Biology

Turtles and tortoises are in trouble

Turtles and tortoises (chelonians) have been integral components of global ecosystems for about 220 million years and have played important roles in human culture for at least 400,000 years. The chelonian shell is a remarkable evolutionary adaptation, facilitating success in terrestrial, freshwater and marine ecosystems. Today, more than half of the 360 living species and 482 total taxa (species and subspecies combined) are threatened with extinction. This places chelonians among the groups with the highest extinction risk of any sizeable vertebrate group. Turtle populations are declining rapidly due to habitat loss, consumption by humans for food and traditional medicines and collection for the international pet trade. Many taxa could become extinct in this century. Here, we examine survival threats to turtles and tortoises and discuss the interventions that will be needed to prevent widespread extinction in this group in coming decades.

Current Biology

Wave-like patterns of plant phenology determine ungulate movement tactics

Animals exhibit a diversity of movement tactics [1]. Tracking resources that change across space and time is predicted to be a fundamental driver of animal movement [2]. For example, some migratory ungulates (i.e., hooved mammals) closely track the progression of highly nutritious plant green-up, a phenomenon called “green-wave surfing” [3-5]. Yet, general principles describing how the dynamic nature of resources determine movement tactics are lacking [6]. We tested emerging theory that predicts surfing and the existence of migratory behavior will be favored in environments where green-up is fleeting and moves sequentially across large landscapes (i.e., wave-like green-up) [7]. Landscapes exhibiting wave-like patterns of green-up facilitated surfing and explained the existence of migratory behavior across 61 populations of four ungulate species on two continents (n=1,696 individuals). At the species level, foraging benefits were equivalent between tactics, suggesting that each movement tactic is fine tuned to local patterns of plant phenology. For decades, ecologists have sought to understand how animals move to select habitat, commonly defining habitat as a set of static patches [8, 9]. Our findings indicate that animal movement tactics emerge as a function of the flux of resources across space and time, underscoring the need to redefine habitat to include its dynamic attributes. As global habitats continue to be modified by anthropogenic disturbance and climate change [10], our synthesis provides a generalizable framework to understand how animal movement will be influenced by altered patterns of resource phenology.

Alberta, British Columbia, Idaho, Wyoming

Amphibian mucus triggers a developmental transition in the frog-killing chytrid fungus

The frog-killing chytrid fungus Batrachochytrium dendrobatidis ( Bd ) is decimating amphibian populations around the world. Bd has a biphasic life cycle, alternating between motile zoospores that disperse within aquatic environments and sessile sporangia that grow within the mucus-coated skin of amphibians. Zoospores lack cell walls and swim rapidly through aquatic environments using a posterior flagellum and crawl across solid surfaces using actin structures similar to those of human cells. Bd transitions from this motile dispersal form to its reproductive form by absorbing its flagellum, rearranging its actin cytoskeleton, and rapidly building a chitin-based cell wall—a process called “encystation.” The resulting sporangium increases in volume by two or three orders of magnitude while undergoing rounds of mitosis without cytokinesis to form a large ceonocyte. The sporangium then cellurizes by dividing its cytoplasm into dozens of new zoospores. After exiting the sporangium through a discharge tube onto the amphibian skin, daughter zoospores can then reinfect the same individual or find a new host. Although encystation is critical to Bd growth, whether and how this developmental transition is triggered by external signals was previously unknown. We discovered that exposure to amphibian mucus triggers rapid and reproducible encystation within minutes. This response can be recapitulated with purified mucin, the bulk component of mucus, but not by similarly viscous methylcellulose or simple sugars. Mucin-induced encystation does not require gene expression but does require surface adhesion, calcium signaling, and modulation of the actin cytoskeleton. Mucus-induced encystation may represent a key mechanism for synchronizing Bd development with the arrival at the host.

Current Biology

Floodplain ecology: A novel wetland community of the Amazon

An expedition to the upper estuarine reaches of the Amazon River reveals intriguing overlap of tropical mangrove wetlands with riverine floodplain forests. This newly discovered type of forested wetland assemblage may provide a uniquely process-rich carbon hotspot.

Amazon River

New frontiers in bird migration research

Bird migrations are impressive behavioral phenomena, representing complex spatiotemporal strategies to balance costs of living while maximizing fitness. The field of bird migration research has made great strides over the past decades, yet fundamental gaps remain. Technologies have sparked a transformation in the study of bird migration research by revealing remarkable insights into the underlying behavioral, cognitive, physiological and evolutionary mechanisms of these diverse journeys. Here, we aim to encourage broad discussions and promote future studies by highlighting research fields that are characterized by major knowledge gaps or conflicting evidence, namely the fields of navigation, social learning, individual development, energetics and conservation. We approach each topic by summarizing the current state of knowledge and provide a future outlook of ideas and state-of-the-art methods to further advance the field. Integrating knowledge across these disciplines will allow us to understand the adaptive abilities of different species and to develop effective conservation strategies in a rapidly changing world.

Current Biology

Genetic architecture and evolution of color variation in American black bears

Color variation is a frequent evolutionary substrate for camouflage in small mammals, but the underlying genetics and evolutionary forces that drive color variation in natural populations of large mammals are mostly unexplained. The American black bear, Ursus americanus ( U. americanus ), exhibits a range of colors including the cinnamon morph, which has a similar color to the brown bear, U. arctos , and is found at high frequency in the American southwest. Reflectance and chemical melanin measurements showed little distinction between U. arctos and cinnamon U. americanus individuals. We used a genome-wide association for hair color as a quantitative trait in 151 U. americanus individuals and identified a single major locus (p < 10 −13 ). Additional genomic and functional studies identified a missense alteration (R153C) in Tyrosinase-related protein 1 ( TYRP1 ) that likely affects binding of the zinc cofactor, impairs protein localization, and results in decreased pigment production. Population genetic analyses and demographic modeling indicated that the R153C variant arose 9.36 kya in a southwestern population where it likely provided a selective advantage, spreading both northwards and eastwards by gene flow. A different TYRP1 allele, R114C, contributes to the characteristic brown color of U. arctos but is not fixed across the range.

Current Biology

Population genomics of recovery and extinction in Hawaiian honeycreepers

Native Hawaiian forest birds are experiencing an unprecedented extinction crisis. In particular, the iconic Hawaiian honeycreeper radiation has declined to just 17 out of ∼60 species remaining, most threatened with extinction due to avian malaria. Here, we investigate the genomic signatures of these declines in three honeycreeper species: the critically endangered ʻakikiki ( Oreomystis bairdi ) and ʻakekeʻe ( Loxops caeruleirostris ) and the extinct poʻouli ( Melamprosops phaeosoma ). Surprisingly, we find that Hawaiian honeycreepers, even the last known po‘ouli individual, maintain high heterozygosity compared with other island birds, reflecting historically large population sizes. This high heterozygosity may contribute to an elevated impact of inbreeding depression, as evidenced by reduced survival and reproductive success among highly inbred ‘akikiki. Demographic analysis revealed that recent precipitous declines in ‘akikiki and ‘akekeʻe coincide with the spread of avian malaria in the late 20 th century, consistent with malaria being the primary driver of population collapse. Using predictive population viability modeling, we explore potential recovery scenarios for ʻakekeʻe, which has recently declined below 100 individuals in the wild. Our models predict that, under current conditions, ‘akekeʻe is likely to go extinct in the near future. However, if mosquito control campaigns are effective at reducing malaria, recovery can still occur. These findings emphasize the urgency of ongoing mosquito control efforts, demonstrating hope for a species nearing the brink of extinction. More broadly, our study provides a detailed examination of genomic diversity, inbreeding depression, and extinction risk in a collapsing adaptive radiation, with implications for conservation of other endangered island species.

Hawaii

Foraging benefits promote fitness in migratory mule deer

Although migration is widespread among ungulates, the fitness benefits associated with different migratory tactics have rarely been documented. Here, we evaluated a 9-year dataset on a migratory population of mule deer to test the hypothesis that long-distance migration provides access to seasonal forage which translates into demographic benefits. Mule deer that migrated long (>130 km) and medium distances (50–130 km) accessed higher forage quality and thus gained 1.3–2.7 times more fat over the growing season compared to mule deer that remained year-round as residents within a desert ecosystem. Elevated levels of fat translated to ∼20% higher probability of adult annual survival than residents. Mule deer that remained year-round in the desert portion of the study area were so resource-limited that they raised fawns at the expense of their own survival. Due to their higher levels of fat, annual survival, and fetal rates, migrants showed more robust population growth (λ = 1.03) compared to residents, which exhibited projected declines in population size over time (λ = 0.95). These results support the notion that migration translates into demographic benefits and highlight the urgent conservation work necessary to sustain diverse ungulate migrations amid habitat alteration due to climate change and an expanding web of linear barriers to movement.

Wyoming

Current state of knowledge on biological effects from contaminants on arctic wildlife and fish

Since the last Arctic Monitoring and Assessment Programme (AMAP) effort to review biological effects of the exposure to organohalogen compounds (OHCs) in Arctic biota, there has been a considerable number of new Arctic effect studies. Here, we provide an update on the state of the knowledge of OHC, and also include mercury, exposure and/or associated effects in key Arctic marine and terrestrial mammal and bird species as well as in fish by reviewing the literature published since the last AMAP assessment in 2010. We aimed at updating the knowledge of how single but also combined health effects are or can be associated to the exposure to single compounds or mixtures of OHCs. We also focussed on assessing both potential individual as well as population health impacts using population-specific exposure data post 2000. We have identified quantifiable effects on vitamin metabolism, immune functioning, thyroid and steroid hormone balances, oxidative stress, tissue pathology, and reproduction. As with the previous assessment, a wealth of documentation is available for biological effects in marine mammals and seabirds, and sentinel species such as the sledge dog and Arctic fox, but information for terrestrial vertebrates and fish remain scarce. While hormones and vitamins are thoroughly studied, oxidative stress, immunotoxic and reproductive effects need further investigation. Depending on the species and population, some OHCs and mercury tissue contaminant burdens post 2000 were observed to be high enough to exceed putative risk threshold levels that have been previously estimated for non-target species or populations outside the Arctic. In this assessment, we made use of risk quotient calculations to summarize the cumulative effects of different OHC classes and mercury for which critical body burdens can be estimated for wildlife across the Arctic. As our ultimate goal is to better predict or estimate the effects of OHCs and mercury in Arctic wildlife at the individual, population and ecosystem level, there remain numerous knowledge gaps on the biological effects of exposure in Arctic biota. These knowledge gaps include the establishment of concentration thresholds for individual compounds as well as for realistic cocktail mixtures that in fact indicate biologically relevant, and not statistically determined, health effects for specific species and subpopulations. Finally, we provide future perspectives on understanding Arctic wildlife health using new in vivo, in vitro, and in silico techniques, and provide case studies on multiple stressors to show that future assessments would benefit from significant efforts to integrate human health, wildlife ecology and retrospective and forecasting aspects into assessing the biological effects of OHC and mercury exposure in Arctic wildlife and fish.

Science of the Total Environment

An assessment of current wolf Canis lupus domestication hypotheses based on wolf ecology and behaviour

The dog was the first domesticated animal. Its derivation from grey wolves Canis lupus is important to the study of mammalian domestication, and wolf domestication is an active area of investigation. Recent popular books have promoted a hypothesis that wolves domesticated themselves as opposed to the earliest hypothesis that featured pup collection, adoption, and artificial selection. Continuing research has produced a greater understanding of wolf ecology and behaviour, including new insights into the wolf’s interaction with humans. Several characteristics make the wolf conducive to domestication: its sociality, catholic diet, excellent individual and cultural memory, inbreeding tolerance, varied personalities, and adaptable lifestyle. The wolf’s fear of humans is the main impediment and that alone is a factor strongly disfavouring the self-selection hypothesis. However, collecting young pups from dens and raising them would foster their socialising with humans as pack members. Neither hypothesis explains how wolves undergoing domestication were separated reproductively from their wild relatives, an important condition for domestication. We combine information from the literature with information from our own research on wild wolves, archaeology, and canid morphology. We explain how pup collection and deliberate or incidental selection and encouragement to breed with similarly raised wolves could keep incipient dogs separated reproductively from wild relatives. The key is humans regularly feeding the wolves and keeping only those able to live harmoniously with humans. Well-fed, human-dependent wolves would remain near their food supply and in the company of humans, thus increasing their bonds to humans and vice versa . Outbreeding with wild wolves would thus be avoided. Generation after generation of these human-fed, raised, and selected wolves would become increasingly dependent on humans and shaped by them. The pup-adoption hypothesis presented here is more in keeping with basic wolf ecology and behaviour than the self-domestication hypothesis.

Current Biology

Uncertainty in spatially explicit animal dispersal models

Uncertainty in estimates of survival of dispersing animals is a vexing difficulty in conservation biology. The current notion is that this uncertainty decreases the usefulness of spatially explicit population models in particular. We examined this problem by comparing dispersal models of three levels of complexity: (1) an event-based binomial model that considers only the occurrence of mortality or arrival, (2) a temporally explicit exponential model that employs mortality and arrival rates, and (3) a spatially explicit grid-walk model that simulates the movement of animals through an artificial landscape. Each model was fitted to the same set of field data. A first objective of the paper is to illustrate how the maximum-likelihood method can be used in all three cases to estimate the means and confidence limits for the relevant model parameters, given a particular set of data on dispersal survival. Using this framework we show that the structure of the uncertainty for all three models is strikingly similar. In fact, the results of our unified approach imply that spatially explicit dispersal models, which take advantage of information on landscape details, suffer less from uncertainly than do simpler models. Moreover, we show that the proposed strategy of model development safeguards one from error propagation in these more complex models. Finally, our approach shows that all models related to animal dispersal, ranging from simple to complex, can be related in a hierarchical fashion, so that the various approaches to modeling such dispersal can be viewed from a unified perspective.

Ecological Applications

The role of vermetid gastropods in the development of the Florida Middle Ground, northeast Gulf of Mexico

The Florida Middle Ground is a complex of north to northwest trending ridges that lie approximately 180 km northwest of Tampa Bay, Florida. The irregular ridges appear on the otherwise gently sloping West Florida shelf and exhibit between 10-15 m of relief. Modern studies interpret the ridges as remnants of a Holocene coral-reef buildup that today provide a hard substrate for growth of a variety of benthic organisms including hydrocorals, scleractinians, alcyonarians, and algae. Recent rotary coring reveals that the core of the eastern ridge of the Florida Middle Ground complex consists of unconsolidated marine calcareous muddy sand that is capped by a boundstone composed primarily of the sessile vermetid gastropod Petaloconchus sp., and overlays a weathered, fossiliferous limestone. Accelerator Mass Spectrometry radiocarbon ages (uncalibrated) on the 3.6-m thick vermetid worm rock indicate that it developed during a sea-level stillstand in the early Holocene (8,225 &plusmn;30-8,910 &plusmn; 25 yr B.P.). Our observations suggest that the Florida Middle Ground is a remnant of a series of shore parallel bars that formed in the early Holocene and were capped by a 3.6-m thick unit of vermetid gastropods. During a rapid sea-level rise that began ~8,000 yr B.P. the vermetids growth ceased and the worm rock preserved the ridges structure. Diver observations document that the edges of the ridges are currently being eroded and undermined by biological activity and current action, leading to calving of large capstone blocks.

Florida

New studies initiated by the U.S. Geological Survey - Effects of nutrient enrichment on stream ecosystems

In 2001, the U.S. Geological Survey’s National Water-Quality Assessment (NAWQA) Program began an intensive study of nutrient enrichment elevated concentrations of nitrogen and phosphorus in streams in five agricultural basins across the Nation (see map, p. 2). This study is providing nationally consistent and comparable data and analyses of nutrient conditions, including how these conditions vary as a result of natural and human-related factors, and how nutrient conditions affect algae and other biological communities. This information will benefit stakeholders, including the U.S. Environmental Protection Agency (USEPA) and its partners, who are developing nutrient criteria to protect the aquatic health of streams in different geographic regions. Nutrient enrichment is one of five national priority topics addressed by NAWQA in its second decade of studies, which began in 2001. During its first round of assessments in 51 major river basins (referred to as “Study Units”), NAWQA scientists collected data on water chemistry, stream hydrology and habitat, and biological communities; currently, NAWQA is revisiting selected basins and focusing on (1) trends, (2) factors that affect water quality and aquatic health, and (3) national priority water issues related to, for example, the development of nutrient criteria, source-water protection strategies, and stream restoration plans. The nutrient enrichment study has four major objectives that address nutrient conditions, dissolved oxygen, aquatic communities, and geographic and landscape features in agricultural basins (see inset). The focus on agricultural streams is a starting point. As the study progresses, streams draining other land uses, such as those in residential and urban areas, will likely be added.

Fact Sheet

Space-based monitoring of penguin diet links sea ice, food webs, and population change

Rapid environmental change is reshaping Antarctic ecosystems through shifts in temperature and sea ice dynamics, with implications for species such as the iconic Adélie penguin ( Pygoscelis adeliae ). Because Antarctic predators rely on a relatively small number of key prey resources in the region 1 whose life histories are intrinsically linked to sea ice, 2 , 3 these abiotic changes are expected to cascade through food webs. However, the scale and remoteness of Antarctica have limited efforts to link environmental change to ecological responses across the continent. Combining tools from imaging spectroscopy, stable isotope analysis, and hierarchical statistical modeling, we reconstructed Adélie penguin diet across the entirety of the species’ global range over a three-decade period (1984–2013) using satellite imagery from the Landsat program. This approach leveraged the distinct spectral properties (a generalized measure of color) of penguin guano as observed by satellites, 4 , 5 which vary according to penguin diet. 6 , 7 We found pronounced differences in diet across the continent and that year-to-year dietary shifts were strongly associated with sea ice dynamics. Higher sea ice corresponded to more fish-based diets, whereas lower sea ice was associated with a greater reliance on krill. Additionally, spatial differences in penguin diet were associated with long-term trends in penguin abundance, linking food web processes to large-scale population dynamics. This study represents the first use of satellite observations to capture trophic dynamics at continental and decadal scales and highlights how environmental change might restructure Antarctic food webs and influence the future of a key sentinel species.

Current Biology