Fitting individual-based models of spatial population dynamics to long-term monitoring data.

Generating spatial predictions of species distribution is a central task for research and policy. Currently, correlative species distribution models (cSDMs) are among the most widely used tools for this purpose. However, a fundamental assumption of cSDMs, that species distributions are in equilibrium with their environment, is rarely fulfilled in real data and limits the applicability of cSDMs for dynamic projections. Process-based, dynamic SDMs (dSDMs) promise to overcome these limitations as they explicitly represent transient dynamics and enhance spatiotemporal transferability. Software tools for implementing dSDMs are becoming increasingly available, but their parameter estimation can be complex. Here, we test the feasibility of calibrating and validating a dSDM using long-term monitoring data of Swiss red kites (Milvus milvus). This population has shown strong increases in abundance and a progressive range expansion over the last decades, indicating a nonequilibrium situation. We construct an individual-based model using the RangeShiftR modeling platform and use Bayesian inference for model calibration. This allows the integration of heterogeneous data sources, such as parameter estimates from published literature and observational data from monitoring schemes, with a coherent assessment of parameter uncertainty. Our monitoring data encompass counts of breeding pairs at 267 sites across Switzerland over 22 years. We validate our model using a spatial-block cross-validation scheme and assess predictive performance with a rank-correlation coefficient. Our model showed very good predictive accuracy of spatial projections and represented well the observed population dynamics over the last two decades. Results suggest that reproductive success was a key factor driving the observed range expansion. According to our model, the Swiss red kite population fills large parts of its current range but has potential for further increases in density. We demonstrate the practicality of data integration and validation for dSDMs using RangeShiftR. This approach can improve predictive performance compared to cSDMs. The workflow presented here can be adopted for any population for which some prior knowledge on demographic and dispersal parameters as well as spatiotemporal observations of abundance or presence/absence are available. The fitted model provides improved quantitative insights into the ecology of a species, which can greatly aid conservation and management efforts.

Natal legacies cause social and spatial marginalization during dispersal.

Early-life experiences can drive subsequent variation in social behaviours, but how differences among individuals emerge remains unknown. We combined experimental manipulations with GPS-tracking to investigate the pathways through which developmental conditions affect social network position during the early dispersal of wild red kites (Milvus milvus). Across 211 juveniles from 140 broods, last-hatched chicks-the least competitive-had the fewest number of peer encounters after fledging. However, when food supplemented, they had more encounters than all others. Using 4425 bird-days of GPS data, we revealed that this was driven by differential responses to competition, with less competitive individuals naturally spreading out into marginal areas, and clustering in central foraging areas when food supplemented. Our results suggest that early-life adversities can cause significant natal legacies on individual behaviour beyond independence, with potentially far-reaching consequences on the social and spatial structure of animal populations.

Sex and size shape the ontogeny of partial migration.

The arrival-time hypothesis of partial seasonal migration proposes that over-winter residence is driven by reproductive benefits of early presence on the breeding grounds. Thus, it predicts increased occurrence of residence at reproductive age. In contrast, the body size hypothesis proposes age-independent benefits of residence for large individuals, who should exhibit greater winter tolerance. Despite different expectations in age patterns for the two hypotheses in long-lived partially migrant species, there is little empirical work investigating the ontogeny of migratory phenotypic expression, that is the expression of residence or migration. We investigated the influence of age, sex and body size on migratory phenotype throughout ontogeny (from first year to early adulthood) in a long-lived partially migrant species, the red kite Milvus milvus. We GPS-tracked 311 individuals tagged as juveniles and 70 individuals tagged as adults over multiple years, yielding 881 observed annual cycles. From this data, we estimated age-dependent probabilities of the transition to residence and of survival in migrants and residents using a Bayesian multistate capture-recapture model, as well as the probability of resuming migration once resident. We then calculated the resulting proportion of residents per age class. In both sexes, almost all juveniles migrated in their first winter, after which the probability of becoming resident gradually increased with age class to approximately 0.3 in adults (>3 calendar years). A size effect in third calendar year females suggests that large females adopt residence earlier in life than small females. The transition from residence back to migration only occurred with a probability of 0.15 across all resident individuals. In addition, survival was notably reduced in adult male migrants compared to adult male residents. These results are largely consistent with the arrival-time and body size hypotheses, simultaneously. Our results reveal a plastic, yet primarily directional within-individual change in migratory phenotype towards more residence with increasing age, varying between sexes and between individuals of different size. This study highlights that different individual characteristics can jointly shape the ontogeny of migratory behaviour and result in complex within-population patterns and persistence of migratory phenotypes.

Turning tables: food availability shapes dynamic aggressive behaviour among asynchronously hatching siblings in red kites Milvus milvus.

Aggression represents the backbone of dominance acquisition in several animal societies, where the decision to interact is dictated by its relative cost. Among siblings, such costs are weighted in the light of inclusive fitness, but how this translates to aggression patterns in response to changing external and internal conditions remains unclear. Using a null-model-based approach, we investigate how day-to-day changes in food provisioning affect aggression networks and food allocation in growing red kite (Milvus milvus) nestlings, whose dominance rank is largely dictated by age. We show that older siblings, irrespective of age, change from targeting only close-aged peers (close-competitor pattern) when food provisioning is low, to uniformly attacking all other peers (downward heuristic pattern) as food conditions improve. While food allocation was generally skewed towards the older siblings, the youngest sibling in the nest increased its probability of accessing food as more was provisioned and as downward heuristic patterns became more prominent, suggesting that different aggression patterns allow for catch-up growth after periods of low food. Our results indicate that dynamic aggression patterns within the nest modulate environmental effects on juvenile development by influencing the process of dominance acquisition and potentially impacting the fledging body condition, with far-reaching fitness consequences.

Climate-driven variation in dispersal ability predicts responses to forest fragmentation in birds.

Species sensitivity to forest fragmentation varies latitudinally, peaking in the tropics. A prominent explanation for this pattern is that historical landscape disturbance at higher latitudes has removed fragmentation-sensitive species or promoted the evolution of more resilient survivors. However, it is unclear whether this so-called extinction filter is the dominant driver of geographic variation in fragmentation sensitivity, particularly because climatic factors may also cause latitudinal gradients in dispersal ability, a key trait mediating sensitivity to habitat fragmentation. Here we combine field survey data with a morphological proxy for avian dispersal ability (hand-wing index) to assess responses to forest fragmentation in 1,034 bird species worldwide. We find that fragmentation sensitivity is strongly predicted by dispersal limitation and that other factors-latitude, body mass and historical disturbance events-have relatively limited explanatory power after accounting for species differences in dispersal. We also show that variation in dispersal ability is only weakly predicted by historical disturbance and more strongly associated with intra-annual temperature fluctuations (seasonality). Our results suggest that climatic factors play a dominant role in driving global variation in the impacts of forest fragmentation, emphasizing the need for more nuanced environmental policies that take into account local context and associated species traits.

Pollinator foraging tactics have divergent consequences for the mating system of a tropical plant.

Resolving the consequences of pollinator foraging behaviour for plant mating systems is a fundamental challenge in evolutionary ecology. Pollinators may adopt particular foraging tactics: complete trapline foraging (repeated movements along a fixed route), sample-and-shift trapline foraging (a variable route that incorporates information from previous experiences) and territorial foraging (stochastic movements within a restricted area). Studies that integrate these pollinator foraging tactics with plant mating systems are generally lacking. We investigate the consequences of particular pollinator foraging tactics for Heliconia tortuosa. We combine parentage and sibship inference analysis with simulation modelling to: estimate mating system parameters; infer the foraging tactic adopted by the pollinators; and quantify the impact of pollinator foraging tactics on mating system parameters. We found high outcrossing rates, ubiquitous multiple paternity and a pronounced departure from near-neighbour mating. We also found that plants repeatedly receive pollen from a series of particular donors. We infer that the pollinators primarily adopt complete trapline foraging and occasionally engage in sample-and-shift trapline foraging. This enhances multiple paternity without a substantial increase in near-neighbour mating. The particular pollinator foraging tactics have divergent consequences for multiple paternity and near-neighbour mating. Thus, pollinator foraging behaviour is an important driver of the ecology and evolution of plant mating systems.

Elevated inbreeding in Heliconia tortuosa is determined by tropical forest stand age, isolation and loss of hummingbird functional diversity.

Forest conversion and habitat loss are major threats to biological diversity. Forest regeneration can mitigate the negative effects of old-growth forest loss on species diversity, but less is known about the extent to which forest loss reduces genetic diversity in remnant populations and whether secondary forests play a role in the maintenance of genetic diversity. We quantified genetic diversity in a tropical hummingbird-pollinated understorey herb, Heliconia tortuosa, across a landscape mosaic of primary and secondary forest regrowth. Using microsatellite genotypes from >850 adult and juvenile plants within 33 forest patches and extensive bird surveys, we examined the effect of contemporary and historical landscape features including forest age (primary vs. secondary forest), stand isolation and pollinator assemblages on genetic diversity and levels of inbreeding in H. tortuosa. We found that inbreeding was up to three times higher in secondary forest, and this effect was amplified with reductions in primary forest in the surrounding landscape through reduced observed heterozygosity in isolated fragments. Inbreeding in forest patches was negatively correlated with the local frequency of specialist long-distance foraging traplining hummingbirds. Traplining hummingbirds therefore appear to facilitate mating among unrelated plants-an inference we tested using empirically parameterized simulations. Higher levels of inbreeding in H. tortuosa are therefore associated with reduced functional diversity of hummingbirds in secondary forests and forest patches isolated from primary forests. Our findings suggest a cryptic consequence of primary forest loss and secondary forest regeneration through the disruption of mutualistic interactions resulting in the erosion of genetic diversity in a common understorey plant.

Hungry or angry? Experimental evidence for the effects of food availability on two measures of stress in developing wild raptor nestlings.

Food shortage challenges the development of nestlings; yet, to cope with this stressor, nestlings can induce stress responses to adjust metabolism or behaviour. Food shortage also enhances the antagonism between siblings, but it remains unclear whether the stress response induced by food shortage operates via the individual nutritional state or via the social environment experienced. In addition, the understanding of these processes is hindered by the fact that effects of food availability often co-vary with other environmental factors. We used a food supplementation experiment to test the effect of food availability on two complementary stress measures, feather corticosterone (CORTf) and heterophil/lymphocyte ratio (H/L) in developing red kite (Milvus milvus) nestlings, a species with competitive brood hierarchy. By statistically controlling for the effect of food supplementation on the nestlings' body condition, we disentangled the effects of food and ambient temperature on nestlings during development. Experimental food supplementation increased body condition, and both CORTf and H/L were reduced in nestlings of high body condition. Additionally, CORTf decreased with age in non-supplemented nestlings. H/L decreased with age in all nestlings and was lower in supplemented last-hatched nestlings compared with non-supplemented ones. Ambient temperature showed a negative effect on H/L. Our results indicate that food shortage increases the nestlings' stress levels through a reduced food intake affecting both their nutritional state and their social environment. Thus, food availability in conjunction with ambient temperature shapes between- and within-nest differences in stress load, which may have carry-over effects on behaviour and performance in further life-history stages.

Weather and food availability additively affect reproductive output in an expanding raptor population.

The joint effects of interacting environmental factors on key demographic parameters can exacerbate or mitigate the separate factors' effects on population dynamics. Given ongoing changes in climate and land use, assessing interactions between weather and food availability on reproductive performance is crucial to understand and forecast population dynamics. By conducting a feeding experiment in 4 years with different weather conditions, we were able to disentangle the effects of weather, food availability and their interactions on reproductive parameters in an expanding population of the red kite (Milvus milvus), a conservation-relevant raptor known to be supported by anthropogenic feeding. Brood loss occurred mainly during the incubation phase, and was associated with rainfall and low food availability. In contrast, brood loss during the nestling phase occurred mostly due to low temperatures. Survival of last-hatched nestlings and nestling development was enhanced by food supplementation and reduced by adverse weather conditions. However, we found no support for interactive effects of weather and food availability, suggesting that these factors affect reproduction of red kites additively. The results not only suggest that food-weather interactions are prevented by parental life-history trade-offs, but that food availability and weather conditions are crucial separate determinants of reproductive output, and thus population productivity. Overall, our results suggest that the observed increase in spring temperatures and enhanced anthropogenic food resources have contributed to the elevational expansion and the growth of the study population during the last decades.

Reconciling biodiversity with timber production and revenue via an intensive forest management experiment.

Understanding how land-management intensification shapes the relationships between biodiversity, yield, and economic benefit is critical for managing natural resources. Yet, manipulative experiments that test how herbicides affect these relationships are scarce, particularly in forest ecosystems where considerable time lags exist between harvest revenue and initial investments. We assessed these relationships by combining 7 yr of biodiversity surveys (>800 taxa) and forecasts of timber yield and economic return from a replicated, large-scale experiment that manipulated herbicide application intensity in operational timber plantations. Herbicides reduced species richness across trophic groups (-18%), but responses by higher-level trophic groups were more variable (0-38% reduction) than plant responses (-40%). Financial discounting, a conventional economic method to standardize past and future cash flows, strongly modified biodiversity-revenue relationships caused by management intensity. Despite a projected 28% timber yield gain with herbicides, biodiversity-revenue trade-offs were muted when opportunity costs were high (i.e., economic discount rates ≥7%). Although herbicides can drive biodiversity-yield trade-offs, under certain conditions, financial discounting provides opportunities to reconcile biodiversity conservation with revenue.

When are hypotheses useful in ecology and evolution?

Research hypotheses have been a cornerstone of science since before Galileo. Many have argued that hypotheses (1) encourage discovery of mechanisms, and (2) reduce bias-both features that should increase transferability and reproducibility. However, we are entering a new era of big data and highly predictive models where some argue the hypothesis is outmoded. We hypothesized that hypothesis use has declined in ecology and evolution since the 1990s, given the substantial advancement of tools further facilitating descriptive, correlative research. Alternatively, hypothesis use may have become more frequent due to the strong recommendation by some journals and funding agencies that submissions have hypothesis statements. Using a detailed literature analysis (N = 268 articles), we found prevalence of hypotheses in eco-evo research is very low (6.7%-26%) and static from 1990-2015, a pattern mirrored in an extensive literature search (N = 302,558 articles). Our literature review also indicates that neither grant success nor citation rates were related to the inclusion of hypotheses, which may provide disincentive for hypothesis formulation. Here, we review common justifications for avoiding hypotheses and present new arguments based on benefits to the individual researcher. We argue that stating multiple alternative hypotheses increases research clarity and precision, and is more likely to address the mechanisms for observed patterns in nature. Although hypotheses are not always necessary, we expect their continued and increased use will help our fields move toward greater understanding, reproducibility, prediction, and effective conservation of nature.

Do birds help trees grow? An experimental study of the effects of land-use intensification on avian trophic cascades.

By regulating populations of herbivores, predators can indirectly influence plant production. However, the factors influencing the strength of this type of trophic cascade are still unclear. We hypothesized that changes to plant community structure would affect the number of avian predators, thereby mediating cascade strength. Using a 4-yr, blocked, split-plot experiment, we independently manipulated both predators (birds) and plants in an early seral managed forest system in western Oregon, USA, and measured abundance across three trophic levels. We applied herbicides, as a surrogate for land-use intensification, to recently clear-cut stands to establish an experimental gradient in plant abundance and species richness, and excluded birds using 28, 225 m2 exclosures. In total, we counted and identified 94,738 arthropods of 141 families in paired control and bird exclosure plots. On average, insectivorous birds reduced arthropod abundance by 16% and plant damage by 14%, and some well-known pests (e.g., Adelges cooleyi) of crop trees (mostly Pseudotsuga menziesii) in our system were reduced by as much as 30%. However, this effect did not translate into a trophic cascade that increased crop-tree growth in the presence of birds. We experimentally reduced plant abundance and diversity by 67% and 55%, respectively, in the most intensive herbicide treatment in relation to untreated controls, but reduced vegetative resources did not change the strength of the direct effect of birds on arthropods or the indirect effect of birds on plants.

Extinction filters mediate the global effects of habitat fragmentation on animals.

Habitat loss is the primary driver of biodiversity decline worldwide, but the effects of fragmentation (the spatial arrangement of remaining habitat) are debated. We tested the hypothesis that forest fragmentation sensitivity-affected by avoidance of habitat edges-should be driven by historical exposure to, and therefore species' evolutionary responses to disturbance. Using a database containing 73 datasets collected worldwide (encompassing 4489 animal species), we found that the proportion of fragmentation-sensitive species was nearly three times as high in regions with low rates of historical disturbance compared with regions with high rates of disturbance (i.e., fires, glaciation, hurricanes, and deforestation). These disturbances coincide with a latitudinal gradient in which sensitivity increases sixfold at low versus high latitudes. We conclude that conservation efforts to limit edges created by fragmentation will be most important in the world's tropical forests.

The Landscape Genetic Signature of Pollination by Trapliners: Evidence From the Tropical Herb, Heliconia tortuosa.

Animal-mediated pollination is essential for the maintenance of plant reproduction, especially in tropical ecosystems, where pollination networks have been thought to have highly generalized structures. However, accumulating evidence suggests that not all floral visitors provide equally effective pollination services, potentially reducing the number of realized pollinators and increasing the cryptic specialization of pollination networks. Thus, there is a need to understand how different functional groups of pollinators influence pollination success. Here, we examined whether patterns of contemporary pollen-mediated gene flow in Heliconia tortuosa are consistent with the foraging strategy of its territorial or traplining hummingbird pollinators. Territorial hummingbirds defend clumps of flowers and are expected to transfer pollen locally. In contrast, traplining hummingbirds forage across longer distances, thereby increasing pollen flow among forest fragments, and are thought to repeatedly visit particular plants. If trapliners indeed visit the same plants repeatedly along their regular routes, this could lead to a situation where neighboring plants sample genetically distinct pollen pools. To test this hypothesis, we genotyped 720 seeds and 71 mother plants from 18 forest fragments at 11 microsatellite loci. We performed TwoGener analysis to test pollen pool differentiation within sites (among neighboring plants within the same forest fragment: Φ SC ) and between sites (among forest fragments: Φ CT ). We found strong, statistically significant pollen pool differentiation among neighboring mother plants (Φ SC = 0.0506), and weaker, statistically significant differentiation among sites (Φ CT = 0.0285). We interpret this pattern of hierarchical pollen pool differentiation as the landscape genetic signature of the foraging strategy of traplining hummingbirds, where repeatable, long-distance, and high-fidelity routes transfer pollen among particular plants. Although H. tortuosa is also visited by territorial hummingbirds, our results suggest that these pollinators do not contribute substantially to successful pollination, highlighting differences in realized pollination efficiency. This cryptic reduction in the number of realized pollinators potentially increases the vulnerability of pollination success to the decline of populations of traplining hummingbirds, which have been shown to be sensitive to forest fragmentation. We conclude that maintaining habitat connectivity to sustain the foraging routes of trapliners may be essential for the maintenance of pollen-mediated gene flow in human-modified landscapes.

Landscape configurational heterogeneity by small-scale agriculture, not crop diversity, maintains pollinators and plant reproduction in western Europe.

Agricultural intensification is one of the main causes for the current biodiversity crisis. While reversing habitat loss on agricultural land is challenging, increasing the farmland configurational heterogeneity (higher field border density) and farmland compositional heterogeneity (higher crop diversity) has been proposed to counteract some habitat loss. Here, we tested whether increased farmland configurational and compositional heterogeneity promote wild pollinators and plant reproduction in 229 landscapes located in four major western European agricultural regions. High-field border density consistently increased wild bee abundance and seed set of radish (Raphanus sativus), probably through enhanced connectivity. In particular, we demonstrate the importance of crop-crop borders for pollinator movement as an additional experiment showed higher transfer of a pollen analogue along crop-crop borders than across fields or along semi-natural crop borders. By contrast, high crop diversity reduced bee abundance, probably due to an increase of crop types with particularly intensive management. This highlights the importance of crop identity when higher crop diversity is promoted. Our results show that small-scale agricultural systems can boost pollinators and plant reproduction. Agri-environmental policies should therefore aim to halt and reverse the current trend of increasing field sizes and to reduce the amount of crop types with particularly intensive management.

Corridors restore animal-mediated pollination in fragmented tropical forest landscapes.

Tropical biodiversity and associated ecosystem functions have become heavily eroded through habitat loss. Animal-mediated pollination is required in more than 94% of higher tropical plant species and 75% of the world's leading food crops, but it remains unclear if corridors avert deforestation-driven pollination breakdown in fragmented tropical landscapes. Here, we used manipulative resource experiments and field observations to show that corridors functionally connect neotropical forest fragments for forest-associated hummingbirds and increase pollen transfer. Further, corridors boosted forest-associated pollinator availability in fragments by 14.3 times compared with unconnected equivalents, increasing overall pollination success. Plants in patches without corridors showed pollination rates equal to bagged control flowers, indicating pollination failure in isolated fragments. This indicates, for the first time, that corridors benefit tropical forest ecosystems beyond boosting local species richness, by functionally connecting mutualistic network partners. We conclude that small-scale adjustments to landscape configuration safeguard native pollinators and associated pollination services in tropical forest landscapes.

Sixty-Seven Years of Land-Use Change in Southern Costa Rica.

Habitat loss and fragmentation of forests are among the biggest threats to biodiversity and associated ecosystem services in tropical landscapes. We use the vicinity of the Las Cruces Biological Station in southern Costa Rica as a regional case study to document seven decades of land-use change in one of the most intensively studied sites in the Neotropics. Though the premontane wet forest was largely intact in 1947, a wave of immigration in 1952 initiated rapid changes over a short period. Overall forest cover was reduced during each time interval analyzed (1947-1960, 1960-1980, 1980-1997, 1997-2014), although the vast majority of forest loss (>90%) occurred during the first two time intervals (1947-1960, 1960-1980) with an annual deforestation rate of 2.14% and 3.86%, respectively. The rate dropped to <2% thereafter and has been offset by forest recovery in fallow areas more recently, but overall forest cover has continued to decline. Approximately 27.9% of the study area is forested currently. Concomitantly, the region shifted from a single contiguous forest to a series of progressively smaller forest fragments with each successive survey. A strong reduction in the amount of core habitat was paralleled by an increased proportion of edge habitat, due to the irregular shape of many forest fragments. Structural connectivity, however, remains high, with an expansive network of >100 km of linear strips of vegetation within a 3 km radius of the station, which may facilitate landscape-level movement for some species. Despite the extent of forest loss, a substantial number of regional landscape-level studies over the past two decades have demonstrated the persistence of many groups of organisms such as birds and mammals. Nonetheless, the continued decline in the quantity and quality of remaining habitat (~30% of remaining forest is secondary), as well as the threat of an extinction debt (or time lag in species loss), may result in the extirpation of additional species if more proactive conservation measures are not taken to reverse current trends-a pattern that reflects many other tropical regions the world over.

BIOFRAG - a new database for analyzing BIOdiversity responses to forest FRAGmentation.

Habitat fragmentation studies have produced complex results that are challenging to synthesize. Inconsistencies among studies may result from variation in the choice of landscape metrics and response variables, which is often compounded by a lack of key statistical or methodological information. Collating primary datasets on biodiversity responses to fragmentation in a consistent and flexible database permits simple data retrieval for subsequent analyses. We present a relational database that links such field data to taxonomic nomenclature, spatial and temporal plot attributes, and environmental characteristics. Field assessments include measurements of the response(s) (e.g., presence, abundance, ground cover) of one or more species linked to plots in fragments within a partially forested landscape. The database currently holds 9830 unique species recorded in plots of 58 unique landscapes in six of eight realms: mammals 315, birds 1286, herptiles 460, insects 4521, spiders 204, other arthropods 85, gastropods 70, annelids 8, platyhelminthes 4, Onychophora 2, vascular plants 2112, nonvascular plants and lichens 320, and fungi 449. Three landscapes were sampled as long-term time series (>10 years). Seven hundred and eleven species are found in two or more landscapes. Consolidating the substantial amount of primary data available on biodiversity responses to fragmentation in the context of land-use change and natural disturbances is an essential part of understanding the effects of increasing anthropogenic pressures on land. The consistent format of this database facilitates testing of generalizations concerning biologic responses to fragmentation across diverse systems and taxa. It also allows the re-examination of existing datasets with alternative landscape metrics and robust statistical methods, for example, helping to address pseudo-replication problems. The database can thus help researchers in producing broad syntheses of the effects of land use. The database is dynamic and inclusive, and contributions from individual and large-scale data-collection efforts are welcome.