Different currencies for calculating resource phenology result in opposite inferences about trophic mismatches.

Shifts in phenology are among the key responses of organisms to climate change. When rates of phenological change differ between interacting species they may result in phenological asynchrony. Studies have found conflicting patterns concerning the direction and magnitude of changes in synchrony, which have been attributed to biological factors. A hitherto overlooked additional explanation are differences in the currency used to quantify resource phenology, such as abundance and biomass. Studying an insectivorous bird (the sanderling) and its prey, we show that the median date of cumulative arthropod biomass occurred, on average, 6.9 days after the median date of cumulative arthropod abundance. In some years this difference could be as large as 21 days. For 23 years, hatch dates of sanderlings became less synchronized with the median date of arthropod abundance, but more synchronized with the median date of arthropod biomass. The currency-specific trends can be explained by our finding that mean biomass per arthropod specimen increased with date. Using a conceptual simulation, we show that estimated rates of phenological change for abundance and biomass can differ depending on temporal shifts in the size distribution of resources. We conclude that studies of trophic mismatch based on different currencies for resource phenology can be incompatible with each other.

Site-specific length-biomass relationships of arctic arthropod families are critical for accurate ecological inferences.

Arthropods play a crucial role in terrestrial ecosystems, for instance in mediating energy fluxes and in forming the food base for many organisms. To better understand their functional role in such ecosystem processes, monitoring of trends in arthropod biomass is essential. Obtaining direct measurements of the body mass of individual specimens is laborious. Therefore, these data are often indirectly acquired by utilizing allometric length-biomass relationships based on a correlative parameter, such as body length. Previous studies have often used such relationships with a low taxonomic resolution and/or small sample size and/or adopted regressions calibrated in different biomes. Despite the scientific interest in the ecology of arctic arthropods, no site-specific family-level length-biomass relationships have hitherto been published. Here we present 27 family-specific length-biomass relationships from two sites in the High Arctic: Zackenberg in northeast Greenland and Knipovich in north Taimyr, Russia. We show that length-biomass regressions from different sites within the same biome did not affect estimates of phenology but did result in substantially different estimates of arthropod biomass. Estimates of daily biomass at Zackenberg were on average 24% higher when calculated using regressions for Knipovich compared to using regressions for Zackenberg. In addition, calculations of daily arthropod biomass at Zackenberg based on order-level regressions from frequently cited studies in literature revealed overestimations of arthropod biomass ranging from 69.7% to 130% compared to estimates based on regressions for Zackenberg. Our results illustrate that the use of allometric relationships from different sites can significantly alter the biological interpretation of, for instance, the interaction between insectivorous birds and their arthropod prey. We conclude that length-biomass relationships should be locally established rather than being based on global relationships.

Arriving late and lean at a stopover site is selected against in a declining migratory bird population.

Loss and/or deterioration of refuelling habitats have caused population declines in many migratory bird species but whether this results from unequal mortality among individuals varying in migration traits remains to be shown. Based on 13 years of body mass and size data of great knots (Calidris tenuirostris) at a stopover site of the Yellow Sea, combined with resightings of individuals marked at this stopover site along the East Asian-Australasian Flyway, we assessed year to year changes in annual apparent survival rates, and how apparent survival differed between migration phenotypes (i.e. migration timing and fuel stores). The measurements occurred over a period of habitat loss and/or deterioration in this flyway. We found that the annual apparent survival rates of great knots rapidly declined from 2006 to 2018, late-arriving individuals with small fuel stores exhibiting the lowest apparent survival rate. There was an advancement in mean arrival date and an increase in the mean fuel load of stopping birds over the study period. Our results suggest that late-arriving individuals with small fuel loads were selected against. Thus, habitat loss and/or deterioration at staging sites may cause changes in the composition of migratory phenotypes at the population-level.

Sulfur in lucinid bivalves inhibits intake rates of a molluscivore shorebird.

A forager's energy intake rate is usually constrained by a combination of handling time, encounter rate and digestion rate. On top of that, food intake may be constrained when a forager can only process a maximum amount of certain toxic compounds. The latter constraint is well described for herbivores with a limited tolerance to plant secondary metabolites. In sulfidic marine ecosystems, many animals host chemoautotrophic endosymbionts, which store sulfur compounds as an energy resource, potentially making their hosts toxic to predators. The red knot Calidris canutus canutus is a molluscivore shorebird that winters on the mudflats of Banc d'Arguin, where the most abundant bivalve prey Loripes orbiculatus hosts sulfide-oxidizing bacteria. In this system, we studied the potential effect of sulfur on the red knots' intake rates, by offering Loripes with various sulfur content to captive birds. To manipulate toxicity, we starved Loripes for 10 days by removing them from their symbiont's energy source sulfide. As predicted, we found lower sulfur concentrations in starved Loripes. We also included natural variation in sulfur concentrations by offering Loripes collected at two different locations. In both cases lower sulfur levels in Loripes resulted in higher consumption rates in red knots. Over time the red knots increased their intake rates on Loripes, showing their ability to adjust to a higher intake of sulfur.

Mismatch-induced growth reductions in a clade of Arctic-breeding shorebirds are rarely mitigated by increasing temperatures.

In seasonal environments subject to climate change, organisms typically show phenological changes. As these changes are usually stronger in organisms at lower trophic levels than those at higher trophic levels, mismatches between consumers and their prey may occur during the consumers' reproduction period. While in some species a trophic mismatch induces reductions in offspring growth, this is not always the case. This variation may be caused by the relative strength of the mismatch, or by mitigating factors like increased temperature-reducing energetic costs. We investigated the response of chick growth rate to arthropod abundance and temperature for six populations of ecologically similar shorebirds breeding in the Arctic and sub-Arctic (four subspecies of Red Knot Calidris canutus, Great Knot C. tenuirostris and Surfbird C. virgata). In general, chicks experienced growth benefits (measured as a condition index) when hatching before the seasonal peak in arthropod abundance, and growth reductions when hatching after the peak. The moment in the season at which growth reductions occurred varied between populations, likely depending on whether food was limiting growth before or after the peak. Higher temperatures led to faster growth on average, but could only compensate for increasing trophic mismatch for the population experiencing the coldest conditions. We did not find changes in the timing of peaks in arthropod availability across the study years, possibly because our series of observations was relatively short; timing of hatching displayed no change over the years either. Our results suggest that a trend in trophic mismatches may not yet be evident; however, we show Arctic-breeding shorebirds to be vulnerable to this phenomenon and vulnerability to depend on seasonal prey dynamics.

Individual-Level Memory Is Sufficient to Create Spatial Segregation among Neighboring Colonies of Central Place Foragers.

AbstractCentral place foragers often segregate in space, even without signs of direct agonistic interactions. Using parsimonious individual-based simulations, we show that for species with spatial cognitive abilities, individual-level memory of resource availability can be sufficient to cause spatial segregation in the foraging ranges of colonial animals. The shapes of the foraging distributions are governed by commuting costs, the emerging distribution of depleted resources, and the fidelity of foragers to their colonies. When colony fidelity is weak and foragers can easily switch to colonies located closer to favorable foraging grounds, this leads to space partitioning with equidistant borders between neighboring colonies. In contrast, when colony fidelity is strong-for example, because larger colonies provide safety in numbers or individuals are unable to leave-it can create a regional imbalance between resource requirements and resource availability. This leads to nontrivial space-use patterns that propagate through the landscape. Interestingly, while better spatial memory creates more defined boundaries between neighboring colonies, it can lower the average intake rate of the population, suggesting a potential trade-off between an individual's attempt for increased intake and population growth rates.

Global biogeography of chemosynthetic symbionts reveals both localized and globally distributed symbiont groups.

In the ocean, most hosts acquire their symbionts from the environment. Due to the immense spatial scales involved, our understanding of the biogeography of hosts and symbionts in marine systems is patchy, although this knowledge is essential for understanding fundamental aspects of symbiosis such as host-symbiont specificity and evolution. Lucinidae is the most species-rich and widely distributed family of marine bivalves hosting autotrophic bacterial endosymbionts. Previous molecular surveys identified location-specific symbiont types that "promiscuously" form associations with multiple divergent cooccurring host species. This flexibility of host-microbe pairings is thought to underpin their global success, as it allows hosts to form associations with locally adapted symbionts. We used metagenomics to investigate the biodiversity, functional variability, and genetic exchange among the endosymbionts of 12 lucinid host species from across the globe. We report a cosmopolitan symbiont species, Candidatus Thiodiazotropha taylori, associated with multiple lucinid host species. Ca. T. taylori has achieved more success at dispersal and establishing symbioses with lucinids than any other symbiont described thus far. This discovery challenges our understanding of symbiont dispersal and location-specific colonization and suggests both symbiont and host flexibility underpin the ecological and evolutionary success of the lucinid symbiosis.

Exploring the drivers of variation in trophic mismatches: A systematic review of long-term avian studies.

Many organisms reproduce in seasonal environments, where selection on timing of reproduction is particularly strong as consumers need to synchronize reproduction with the peaked occurrence of their food. When a consumer species changes its phenology at a slower rate than its resources, this may induce a trophic mismatch, that is, offspring growing up after the peak in food availability, potentially leading to reductions in growth and survival. However, there is large variation in the degree of trophic mismatches as well as in its effects on reproductive output.Here, we explore the potential causes for variation in the strength of trophic mismatches in published studies of birds. Specifically, we ask whether the changes in the degree of mismatch that have occurred over time can be explained by a bird's (a) breeding latitude, (b) migration distance, and/or (c) life-history traits.We found that none of these three factors explain changes in the degree of mismatch over time. Nevertheless, food phenology did advance faster at more northerly latitudes, while shifts in bird phenology did not show a trend with latitude.We argue that the lack of support in our results is attributable to the large variation in the metrics used to describe timing of food availability. We propose a pathway to improve the quantification of trophic mismatches, guided by a more rigorous understanding of links between consumers and their resources.

Comment on "Global pattern of nest predation is disrupted by climate change in shorebirds".

Kubelka et al (Reports, 9 November 2018, p. 680) claim that climate change has disrupted patterns of nest predation in shorebirds. They report that predation rates have increased since the 1950s, especially in the Arctic. We describe methodological problems with their analyses and argue that there is no solid statistical support for their claims.

Morphological and digestive adjustments buffer performance: How staging shorebirds cope with severe food declines.

Organisms cope with environmental stressors by behavioral, morphological, and physiological adjustments. Documentation of such adjustments in the wild provides information on the response space in nature and the extent to which behavioral and bodily adjustments lead to appropriate performance effects. Here we studied the morphological and digestive adjustments in a staging population of migrating Great Knots Calidris tenuirostris in response to stark declines in food abundance and quality at the Yalu Jiang estuarine wetland (northern Yellow Sea, China). At Yalu Jiang, from 2011 to 2017 the densities of intertidal mollusks, the food of Great Knots, declined 15-fold. The staple prey of Great Knots shifted from the relatively soft-shelled bivalve Potamocorbula laevis in 2011-2012 to harder-shelled mollusks such as the gastropod Umbonium thomasi in 2016-2017. The crushing of the mollusks in the gizzard would require a threefold to 11-fold increase in break force. This was partially resolved by a 15% increase in gizzard mass which would yield a 32% increase in shell processing capacity. The consumption of harder-shelled mollusks was also accompanied by reliance on regurgitates to excrete unbreakable parts of prey, rather than the usual intestinal voidance of shell fragments as feces. Despite the changes in digestive morphology and strategy, there was still an 85% reduction in intake rate in 2016-2017 compared with 2011-2012. With these morphological and digestive adjustments, the Great Knots remaining faithful to the staging site to a certain extent buffered the disadvantageous effects of dramatic food declines. However, compensation was not complete. Locally, birds will have had to extend foraging time and use a greater daily foraging range. This study offers a perspective on how individual animals may mitigate the effects of environmental change by morphological and digestive strategies and the limits to the response space of long-distance migrating shorebirds in the wild.

Erratum: Publisher Correction: Resource landscapes explain contrasting patterns of aggregation and site fidelity by red knots at two wintering sites.

[This corrects the article DOI: 10.1186/s40462-018-0142-4.].

Publisher Correction: Fuelling conditions at staging sites can mitigate Arctic warming effects in a migratory bird.

In the original HTML version of this Article, the order of authors within the author list was incorrect. The consortium VRS Castricum was incorrectly listed after Theunis Piersma and should have been listed after Cornelis J. Camphuysen. This error has been corrected in the HTML version of the Article; the PDF version was correct at the time of publication.

Fuelling conditions at staging sites can mitigate Arctic warming effects in a migratory bird.

Under climate warming, migratory birds should align reproduction dates with advancing plant and arthropod phenology. To arrive on the breeding grounds earlier, migrants may speed up spring migration by curtailing the time spent en route, possibly at the cost of decreased survival rates. Based on a decades-long series of observations along an entire flyway, we show that when refuelling time is limited, variation in food abundance in the spring staging area affects fitness. Bar-tailed godwits migrating from West Africa to the Siberian Arctic reduce refuelling time at their European staging site and thus maintain a close match between breeding and tundra phenology. Annual survival probability decreases with shorter refuelling times, but correlates positively with refuelling rate, which in turn is correlated with food abundance in the staging area. This chain of effects implies that conditions in the temperate zone determine the ability of godwits to cope with climate-related changes in the Arctic.

A facultative mutualistic feedback enhances the stability of tropical intertidal seagrass beds.

Marine foundation species such as corals, seagrasses, salt marsh plants, and mangrove trees are increasingly found to engage in mutualistic interactions. Because mutualisms by their very nature generate a positive feedback between the species, subtle environmental impacts on one of the species involved may trigger mutualism breakdown, potentially leading to ecosystem regime shifts. Using an empirically parameterized model, we investigate a facultative mutualism between seagrass and lucinid bivalves with endosymbiotic sulfide-oxidizing gill bacteria in a tropical intertidal ecosystem. Model predictions for our system show that, by alleviating the build-up of toxic sulfide, this mutualism maintains an otherwise intrinsically unstable seagrass ecosystem. However, an increase in seagrass mortality above natural levels, due to e.g. desiccation stress, triggers mutualism breakdown. This pushes the system in collapse-and-recovery dynamics ('slow-fast cycles') characterized by long-term persistent states of bare and seagrass-dominated, with rapid transitions in between. Model results were consistent with remote sensing analyses that suggest feedback-mediated state shifts induced by desiccation. Overall, our combined theoretical and empirical results illustrate the potential of mutualistic feedbacks to stabilize ecosystems, but also reveal an important drawback as small environmental changes may trigger shifts. We therefore suggest that mutualisms should be considered for marine conservation and restoration of seagrass beds.

Stomach fullness shapes prey choice decisions in crab plovers (Dromas ardeola).

Foragers whose energy intake rate is constrained by search and handling time should, according to the contingency model (CM), select prey items whose profitability exceeds or equals the forager's long-term average energy intake rate. This rule does not apply when prey items are found and ingested at a higher rate than the digestive system can process them. According to the digestive rate model (DRM), foragers in such situations should prefer prey with the highest digestive quality, instead of the highest profitability. As the digestive system fills up, the limiting constraint switches from ingestion rate to digestion rate, and prey choice is expected to change accordingly for foragers making decisions over a relative short time window. We use these models to understand prey choice in crab plovers (Dromas ardeola), preying on either small burrowing crabs that are swallowed whole (high profitability, but potentially inducing a digestive constraint) or on larger swimming crabs that are opened to consume only the flesh (low profitability, but easier to digest). To parameterize the CM and DRM, we measured energy content, ballast mass and handling times for different sized prey, and the birds' digestive capacity in three captive individuals. Subsequently, these birds were used in ad libitum experiments to test if they obeyed the rules of the CM or DRM. We found that crab plovers with an empty stomach mainly chose the most profitable prey, matching the CM. When stomach fullness increased, the birds switched their preference from the most profitable prey to the highest-quality prey, matching the predictions of the DRM. This shows that prey choice is context dependent, affected by the stomach fullness of an animal. Our results suggest that prey choice experiments should be carefully interpreted, especially under captive conditions as foragers often 'fill up' in the course of feeding trials.

Resource landscapes explain contrasting patterns of aggregation and site fidelity by red knots at two wintering sites.

BACKGROUND: Space use strategies by foraging animals are often considered to be species-specific. However, similarity between conspecific strategies may also result from similar resource environments. Here, we revisit classic predictions of the relationships between the resource distribution and foragers' space use by tracking free-living foragers of a single species in two contrasting resource landscapes. At two main non-breeding areas along the East-Atlantic flyway (Wadden Sea, The Netherlands and Banc d'Arguin, Mauritania), we mapped prey distributions and derived resource landscapes in terms of the predicted intake rate of red knots (Calidris canutus), migratory molluscivore shorebirds. We tracked the foraging paths of 13 and 38 individual red knots at intervals of 1 s over two and five weeks in the Wadden Sea and at Banc d'Arguin, respectively. Mediated by competition for resources, we expected aggregation to be strong and site fidelity weak in an environment with large resource patches. The opposite was expected for small resource patches, but only if local resource abundances were high. RESULTS: Compared with Banc d'Arguin, resource patches in the Wadden Sea were larger and the maximum local resource abundance was higher. However, because of constraints set by digestive capacity, the average potential intake rates by red knots were similar at the two study sites. Space-use patterns differed as predicted from these differences in resource landscapes. Whereas foraging red knots in the Wadden Sea roamed the mudflats in high aggregation without site fidelity (i.e. grouping nomads), at Banc d'Arguin they showed less aggregation but were strongly site-faithful (i.e. solitary residents). CONCLUSION: The space use pattern of red knots in the two study areas showed diametrically opposite patterns. These differences could be explained from the distribution of resources in the two areas. Our findings imply that intraspecific similarities in space use patterns represent responses to similar resource environments rather than species-specificity. To predict how environmental change affects space use, we need to understand the degree to which space-use strategies result from developmental plasticity and behavioural flexibility. This requires not only tracking foragers throughout their development, but also tracking their environment in sufficient spatial and temporal detail.

Chronobiology of interspecific interactions in a changing world.

Animals should time activities, such as foraging, migration and reproduction, as well as seasonal physiological adaptation, in a way that maximizes fitness. The fitness outcome of such activities depends largely on their interspecific interactions; the temporal overlap with other species determines when they should be active in order to maximize their encounters with food and to minimize their encounters with predators, competitors and parasites. To cope with the constantly changing, but predictable structure of the environment, organisms have evolved internal biological clocks, which are synchronized mainly by light, the most predictable and reliable environmental cue (but which can be masked by other variables), which enable them to anticipate and prepare for predicted changes in the timing of the species they interact with, on top of responding to them directly. Here, we review examples where the internal timing system is used to predict interspecific interactions, and how these interactions affect the internal timing system and activity patterns. We then ask how plastic these mechanisms are, how this plasticity differs between and within species and how this variability in plasticity affects interspecific interactions in a changing world, in which light, the major synchronizer of the biological clock, is no longer a reliable cue owing to the rapidly changing climate, the use of artificial light and urbanization.This article is part of the themed issue 'Wild clocks: integrating chronobiology and ecology to understand timekeeping in free-living animals'.

Diet preferences as the cause of individual differences rather than the consequence.

Behavioural variation within a species is usually explained as the consequence of individual variation in physiology. However, new evidence suggests that the arrow of causality may well be in the reverse direction: behaviours such as diet preferences cause the differences in physiological and morphological traits. Recently, diet preferences were proposed to underlie consistent differences in digestive organ mass and movement patterns (patch residence times) in red knots (Calidris canutus islandica). Red knots are molluscivorous and migrant shorebirds for which the size of the muscular stomach (gizzard) is critical for the food processing rate. In this study, red knots (C. c. canutus, n = 46) were caught at Banc d'Arguin, an intertidal flat ecosystem in Mauritania, and released with radio-tags after the measurement of gizzard mass. Using a novel tracking system (time-of-arrival), patch residence times were measured over a period of three weeks. Whether or not gizzard mass determined patch residence times was tested experimentally by offering 12 of the 46 tagged red knots soft diets prior to release; this reduced an individual's gizzard mass by 20-60%. To validate whether the observed range of patch residence times would be expected from individual diet preferences, we simulated patch residence times as a function of diet preferences via a simple departure rule. Consistent with previous empirical studies, patch residence times in the field were positively correlated with gizzard mass. The slope of this correlation, as well as the observed range of patch residence times, was in accordance with the simulated values. The 12 birds with reduced gizzard masses did not decrease patch residence times in response to the reduction in gizzard mass. These findings suggest that diet preferences can indeed cause the observed among-individual variation in gizzard mass and patch residence times. We discuss how early diet experiences can have cascading effects on the individual expression of both behavioural and physiomorphic traits. This emphasizes that to understand the ecological consequences of individual differences, knowledge of the environment during development is required.

Hampered performance of migratory swans: intra- and inter-seasonal effects of avian influenza virus.

The extent to which animal migrations shape parasite transmission networks is critically dependent on a migrant's ability to tolerate infection and migrate successfully. Yet, sub-lethal effects of parasites can be intensified through periods of increased physiological stress. Long-distance migrants may, therefore, be especially susceptible to negative effects of parasitic infection. Although a handful of studies have investigated the short-term, transmission-relevant behaviors of wild birds infected with low-pathogenic avian influenza viruses (LPAIV), the ecological consequences of LPAIV for the hosts themselves remain largely unknown. Here, we assessed the potential effects of naturally-acquired LPAIV infections in Bewick's swans, a long-distance migratory species that experiences relatively low incidence of LPAIV infection during early winter. We monitored both foraging and movement behavior in the winter of infection, as well as subsequent breeding behavior and inter-annual resighting probability over 3 years. Incorporating data on infection history we hypothesized that any effects would be most apparent in naïve individuals experiencing their first LPAIV infection. Indeed, significant effects of infection were only seen in birds that were infected but lacked antibodies indicative of prior infection. Swans that were infected but had survived a previous infection were indistinguishable from uninfected birds in each of the ecological performance metrics. Despite showing reduced foraging rates, individuals in the naïve-infected category had similar accumulated body stores to re-infected and uninfected individuals prior to departure on spring migration, possibly as a result of having higher scaled mass at the time of infection. And yet individuals in the naïve-infected category were unlikely to be resighted 1 year after infection, with 6 out of 7 individuals that never resighted again compared to 20 out of 63 uninfected individuals and 5 out of 12 individuals in the re-infected category. Collectively, our findings indicate that acute and superficially harmless infection with LPAIV may have indirect effects on individual performance and recruitment in migratory Bewick's swans. Our results also highlight the potential for infection history to play an important role in shaping ecological constraints throughout the annual cycle.

Body shrinkage due to Arctic warming reduces red knot fitness in tropical wintering range.

Reductions in body size are increasingly being identified as a response to climate warming. Here we present evidence for a case of such body shrinkage, potentially due to malnutrition in early life. We show that an avian long-distance migrant (red knot, Calidris canutus canutus), which is experiencing globally unrivaled warming rates at its high-Arctic breeding grounds, produces smaller offspring with shorter bills during summers with early snowmelt. This has consequences half a world away at their tropical wintering grounds, where shorter-billed individuals have reduced survival rates. This is associated with these molluscivores eating fewer deeply buried bivalve prey and more shallowly buried seagrass rhizomes. We suggest that seasonal migrants can experience reduced fitness at one end of their range as a result of a changing climate at the other end.