Urbanization shapes phenotypic selection of fruit traits in a seed-dispersal mutualism.

Urbanization is currently one of the trademarks of the Anthropocene, accelerating evolutionary processes and reshaping ecological interactions over short time scales. Species interactions represent a fundamental pillar of diversity that is being altered globally by anthropogenic change. Urban environments, despite their potential impact, have seldom been studied in relation to how they shape natural selection of phenotypic traits in multispecies interactions. Using a seed-dispersal mutualism as a study system, we estimated the regime and magnitude of phenotypic selection exerted by frugivores on fruit and seed traits across three plant populations with different degrees of urbanization (urban, semiurban, and rural). Urbanization weakened phenotypic selection via an indirect positive impact on fruit production and fitness and, to a lesser extent, through a direct positive effect on species visitation rates. Our results show that urban ecosystems may affect multifarious selection of traits in the short term and highlight the role of humans in shaping eco-evolutionary dynamics of multispecies interactions.

On the adequacy of fruit removal as a proxy for fitness in studies of bird-mediated phenotypic selection.

PREMISE: In fleshy-fruited plants, fruit removal is widely used as a proxy for plant reproductive success. Nevertheless, this proxy may not accurately reflect the number of seeds dispersed, an assumed better proxy for total fitness (fruit removal × mean number of seeds dispersed per fruit). METHODS: We examined under what circumstances fruit removal can be reliable as a proxy for total fitness when assessing bird-mediated selection on fruit traits. In three populations of the Blue Passionflower (Passiflora caerulea), we used the number of fruits pecked per plant as a surrogate for fruit removal to estimate phenotypic selection on fruit and seed traits, and simulations of the effect of the fruit-seed number trade-off on the number of fruits removed. RESULTS: Fruit removal was a good indicator of fitness, accounting for 55 to 68% of the variability in total fitness, measured as total number of seeds removed. Moreover, multivariate selection analyses on fruit crop size, mean fruit diameter and mean seed number using fruit removal as a fitness proxy yielded similar selection regimes to those using total fitness. Simulations showed that producing more fruits, a lower number of seeds per fruit, and a higher variability in seed number can result in a negative relationship between fruit removal and total fitness. CONCLUSIONS: Our results suggest that fruit removal can be reliably used as a proxy for total fitness when (1) there is a weak fruit number-seed number trade-off, (2) fruit crop size and fruit removal correlate positively, and (3) seed number variability does not largely exceed fruit number variability.

Large-scale spatial variability in urban tolerance of birds.

Quantifying intraspecific and interspecific trait variability is critical to our understanding of biogeography, ecology and conservation. But quantifying such variability and understanding the importance of intraspecific and interspecific variability remain challenging. This is especially true of large geographic scales as this is where the differences between intraspecific and interspecific variability are likely to be greatest. Our goal is to address this research gap using broad-scale citizen science data to quantify intraspecific variability and compare it with interspecific variability, using the example of bird responses to urbanization across the continental United States. Using more than 100 million observations, we quantified urban tolerance for 338 species within randomly sampled spatial regions and then calculated the standard deviation of each species' urban tolerance. We found that species' spatial variability in urban tolerance (i.e. standard deviation) was largely explained by the variability of urban cover throughout a species' range (R2  = 0.70). Variability in urban tolerance was greater in species that were more tolerant of urban cover (i.e. the average urban tolerance throughout their range), suggesting that generalist life histories are better suited to adapt to novel anthropogenic environments. Overall, species differences explained most of the variability in urban tolerance across spatial regions. Together, our results indicate that (1) intraspecific variability is largely predicted by local environmental variability in urban cover at a large spatial scale and (2) interspecific variability is greater than intraspecific variability, supporting the common use of mean values (i.e. collapsing observations across a species' range) when assessing species-environment relationships. Further studies, across different taxa, traits and species-environment relationships are needed to test the role of intraspecific variability, but nevertheless, we recommend that when possible, ecologists should avoid using discrete categories to classify species in how they respond to the environment.

Quantifying the relative importance of direct and indirect effects influencing bird nestling growth.

Nestling growth parameters are integral components of avian life-history strategies as they are crucial determinants of individual survival. Although many factors impact on nestling growth, the relative contribution of each one is still debated in the literature. Most studies rely on the assumption that each factor directly affects nestling growth, but indirect effects mediated by other factors are usually the rule in nature. In this study, we present a comprehensive view of both direct and indirect factors affecting nestling growth using the Red-crested Cardinal (Paroaria coronata) as model system. We evaluated the relative importance of different habitat (forest structure), biotic interactions (botfly larvae ectoparasitism, number of siblings, hatching order), and temporal factors (time of breeding) on nestling growth parameters in 278 nestlings of 128 nests by using piecewise structural equation models. We found that botfly ectoparasitism had the strongest direct effect on nestling growth and, in turn, forest structure increased the probability of botfly occurrence. Besides, the interaction between the number of siblings and hatching order influenced nestling growth, indicating that the first and second nestlings had disproportionately higher growth rates in large than in small clutches. Time of breeding also showed a strong positive indirect effect on botfly occurrence, as well as a weak direct positive effect on nestling growth. Our results demonstrate that, under natural conditions, nestling growth is driven by different factors acting not only directly, but also indirectly on this essential life history trait, and that these factors weave a complex web of interrelated variables.

Selection on fruit traits is mediated by the interplay between frugivorous birds, fruit flies, parasitoid wasps and seed-dispersing ants.

Every organism on Earth must cope with a multitude of species interactions both directly and indirectly throughout its life cycle. However, how selection from multiple species occupying different trophic levels affects diffuse mutualisms has received little attention. As a result, how a given species amalgamates the combined effects of selection from multiple mutualists and antagonists to enhance its own fitness remains little understood. We investigated how multispecies interactions (frugivorous birds, ants, fruit flies and parasitoid wasps) generate selection on fruit traits in a seed dispersal mutualism. We used structural equation models to assess whether seed dispersers (frugivorous birds and ants) exerted phenotypic selection on fruit and seed traits in the spiny hackberry (Celtis ehrenbergiana), a fleshy-fruited tree, and how these selection regimes were influenced by fruit fly infestation and wasp parasitoidism levels. Birds exerted negative correlational selection on the combination of fruit crop size and mean seed weight, favouring either large crops with small seeds or small crops with large seeds. Parasitoids selected plants with higher fruit fly infestation levels, and fruit flies exerted positive directional selection on fruit size, which was positively correlated with seed weight. Therefore, higher parasitoidism indirectly correlated with higher plant fitness through increased bird fruit removal. In addition, ants exerted negative directional selection on mean seed weight. Our results show that strong selection on phenotypic traits may still arise in perceived diffuse species interactions. Overall, we emphasize the need to consider diverse direct and indirect partners to achieve a better understanding of the mechanisms driving phenotypic trait evolution in multispecies interactions.

Patrones de herbivoría en Vassobia breviflora (Solanaceae): variación en el daño foliar y selección natural mediada por herbívoros / Patterns of herbivory in Vassobia breviflora (Solanaceae): variation in foliar damage and natural selection mediated by herbivorous

Resumen La selección mediada por herbívoros moldea la evolución de los caracteres defensivos en las plantas. El conocimiento acerca del rol de los herbívoros como mediadores de selección es escaso y más aún si se consideran los grupos funcionales de herbívoros. Los objetivos de este trabajo fueron (1) describir la variación en rasgos foliares entre poblaciones, entre plantas dentro de una población y a nivel sub-individual (intra-planta), (2) explorar la relación entre la variación en el nivel de herbivoría y rasgos foliares, (3) determinar la relación entre rasgos foliares y patrones de daño y (4) estimar los regímenes de selección por diferentes grupos funcionales de herbívoros. Realizamos este estudio en cuatro poblaciones de Vassobia breviflora en el noroeste de Argentina (Yungas). Los rasgos foliares considerados fueron: tamaño, área foliar (af), forma (relación longitud/ancho de la hoja; laf) y proporción de área foliar removida (pafr) (N = 1 582 hojas, 57 plantas). Los herbívoros consumieron 15.6 % del área foliar y 76.8 % de la variación en la pafr ocurrió a nivel sub-individual. El patrón de daño fue dominado por herbívoros cortadores (70 %), seguido de un patrón de herbivoría punteada (22 %), 5 % mixto y 1 % minador. Se detectó selección no lineal para laf (γii = -0.180, EE = 0.76, P < 0.05), y selección correlacional entre el daño cortador y af (γij = -1.297, SE = 0.62, P < 0.05) y entre el daño punteado y af (γij= -1.130, SE=0.76, P < 0.05). La selección natural favoreció plantas con hojas pequeñas y alta remoción foliar y hojas grandes con menor daño y se detectó selección en contra de hojas grandes con mayor daño. Además, deducido de la relación entre el tipo de daño y la adecuación relativa, la selección favorecería el daño punteado por sobre el cortador. Las plantas resolverían el conflicto con los herbívoros según el tipo de daño y la selección natural regularía el despliegue foliar como una estrategia para lidiar con la diversidad de herbívoros.(AU)

Abstract Herbivore mediated-selection shapes the evolution of defensive plant traits. Knowledge about the role of herbivores as mediators of selection is scarce and even more if herbivore functional groups are considered. The objectives of this work were (1) to describe the variation in foliar traits between populations and both between and intra-plants within a population, (2) to explore the relationship between the variation in the herbivory level and foliar traits, (3) to determine the relationship between leaf traits and damage patterns and (4) estimate the selection regimes by different herbivore functional groups. We conducted this study in four populations of Vassobia breviflora in Northwestern Argentina (Yungas). The foliar traits considered were size, leaf area (af), shape (leaf length / width ratio; laf) and proportion of leaf area removed (pafr) (N = 1 582 leaves, 57 plants). The herbivores consumed 15.6 % of the leaf area and 76.8 % of the variation in the pafr occurred at the sub-individual level. The damage pattern was dominated by cutter herbivores (70 %), followed by a dotted herbivory pattern (22 %), mixed 5 % and 1 % miner. Nonlinear selection was detected for laf (γii = -0.180; EE = 0.76; P < 0.05), and correlational selection between the cutter damage and af (γij = -1.297; SE = 0.62; P < 0.05) and between the dotted damage and af (γij = -1.130; SE = 0.76; P < 0.05). Natural selection favored plants with small leaves and high foliar removal and large leaves with less damage and selection against larger leaves with greater damage was detected. In addition, deduced from the relationship between the damage type and the relative fitness, the selection would favor the dotted damage over the cutter one. The plants would resolve the conflict with the herbivores according to the damage type and natural selection would regulate the foliar display as a strategy to deal with the herbivore diversity.(AU)