Limited potential for bird migration to disperse plants to cooler latitudes.

Climate change is forcing the redistribution of life on Earth at an unprecedented velocity1,2. Migratory birds are thought to help plants to track climate change through long-distance seed dispersal3,4. However, seeds may be consistently dispersed towards cooler or warmer latitudes depending on whether the fruiting period of a plant species coincides with northward or southward migrations. Here we assess the potential of plant communities to keep pace with climate change through long-distance seed dispersal by migratory birds. To do so, we combine phenological and migration information with data on 949 seed-dispersal interactions between 46 bird and 81 plant species from 13 woodland communities across Europe. Most of the plant species (86%) in these communities are dispersed by birds migrating south, whereas only 35% are dispersed by birds migrating north; the latter subset is phylogenetically clustered in lineages that have fruiting periods that overlap with the spring migration. Moreover, the majority of this critical dispersal service northwards is provided by only a few Palaearctic migrant species. The potential of migratory birds to assist a small, non-random sample of plants to track climate change latitudinally is expected to strongly influence the formation of novel plant communities, and thus affect their ecosystem functions and community assembly at higher trophic levels.

Frugivore-mediated seed dispersal in fragmented landscapes: Compositional and functional turnover from forest to matrix.

Seed dispersal by frugivores is a fundamental function for plant community dynamics in fragmented landscapes, where forest remnants are typically embedded in a matrix of anthropogenic habitats. Frugivores can mediate both connectivity among forest remnants and plant colonization of the matrix. However, it remains poorly understood how frugivore communities change from forest to matrix due to the loss or replacement of species with traits that are less advantageous in open habitats and whether such changes ultimately influence the composition and traits of dispersed plants via species interactions. Here, we close this gap by using a unique dataset of seed-dispersal networks that were sampled in forest patches and adjacent matrix habitats of seven fragmented landscapes across Europe. We found a similar diversity of frugivores, plants, and interactions contributing to seed dispersal in forest and matrix, but a high turnover (replacement) in all these components. The turnover of dispersed seeds was smaller than that of frugivore communities because different frugivore species provided complementary seed dispersal in forest and matrix. Importantly, the turnover involved functional changes toward larger and more mobile frugivores in the matrix, which dispersed taller, larger-seeded plants with later fruiting periods. Our study provides a trait-based understanding of frugivore-mediated seed dispersal through fragmented landscapes, uncovering nonrandom shifts that can have cascading consequences for the composition of regenerating plant communities. Our findings also highlight the importance of forest remnants and frugivore faunas for ecosystem resilience, demonstrating a high potential for passive forest restoration of unmanaged lands in the matrix.

Predation risk can modify the foraging behaviour of frugivorous carnivores: Implications of rewilding apex predators for plant-animal mutualisms.

Apex predators play key roles in food webs and their recovery can trigger trophic cascades in some ecosystems. Intra-guild competition can reduce the abundances of smaller predators and perceived predation risk can alter their foraging behaviour thereby limiting seed dispersal by frugivorous carnivores. However, little is known about how plant-frugivore mutualisms could be disturbed in the presence of larger predators. We evaluated the top-down effect of the regional superpredator, the Iberian lynx Lynx pardinus, on the number of visits and fruits consumed by medium-sized frugivorous carnivores, as well as the foraging behaviour of identified individuals, by examining the consumption likelihood and the foraging time. We carried out a field experiment in which we placed Iberian pear Pyrus bourgaeana fruits beneath fruiting trees and monitored pear removal by frugivorous carnivores, both inside and outside lynx ranges. Using camera traps, we recorded the presence of the red fox Vulpes vulpes, the Eurasian badger Meles meles and the stone marten Martes foina, as well as the number of fruits they consumed and their time spent foraging. Red fox was the most frequent fruit consumer carnivore. We found there were fewer visits and less fruit consumed by foxes inside lynx ranges, but lynx presence did not seem to affect badgers. We did not observe any stone marten visits inside lynx territories. The foraging behaviour of red foxes was also altered inside lynx ranges whereby foxes were less efficient, consuming less fruit per unit of time and having shorter visits. Local availability of fruit resources, forest coverage and individual personality also were important variables to understand visitation and foraging in a landscape of fear. Our results show a potential trophic cascade from apex predators to primary producers. The presence of lynx can reduce frugivorous carnivore numbers and induce shifts in their feeding behaviour that may modify the seed dispersal patterns with likely consequences for the demography of many fleshy-fruited plant species. We conclude that knowledge of the ecological interactions making up trophic webs is an asset to design effective conservation strategies, particularly in rewilding programs.

Los depredadores ápice juegan papeles clave en las cadenas tróficas y su recuperación puede dar lugar a cascadas tróficas en algunos ecosistemas. La competición intra-gremial puede reducir las abundancias de los depredadores más pequeños y el riesgo de depredación percibido puede alterar su comportamiento de forrajeo, llegando a limitar la dispersión de semillas de los carnívoros frugívoros. Sin embargo, se sabe poco sobre cómo un mutualismo planta-animal podría ser alterado en presencia de grandes depredadores. Aquí evaluamos los efectos en cascada del superdepredador regional, el lince ibérico Lynx pardinus, sobre el número de visitas y frutos consumidos por los carnívoros frugívoros de mediano tamaño, a la vez que el comportamiento de alimentación de individuos identificados, examinando la probabilidad de consumo y el tiempo de forrajeo. Llevamos a cabo un experimento en el que colocamos frutos de piruétano Iberian pear bajo árboles productores y monitoreamos la remoción de peras por los carnívoros frugívoros, tanto dentro como fuera de territorios de lince. Mediante el uso de cámaras trampa, registramos la presencia de zorro rojo Vulpes vulpes, tejón europeo Meles meles y garduña Martes foina, además del número de frutos que consumieron y el tiempo que emplearon forrajeando. El zorro rojo fue el carnívoro consumidor de frutos más frecuente. Encontramos que había menos visitas y un menor consumo de frutos por zorros dentro de los territorios del lince, pero la presencia de lince no pareció afectar a los tejones. No registramos ninguna visita de garduña dentro de los territorios de los linces. El comportamiento de forrajeo de los zorros rojos fue también alterado dentro del rango de distribución del lince, donde los zorros fueron menos eficientes, consumieron menos frutos por unidad de tiempo y realizaron visitas más cortas. La disponibilidad local de frutos, la cobertura forestal y la personalidad individual también fueron variables importantes para entender los patrones de visita y forrajeo en un paisaje del miedo. Nuestros resultados muestran una cascada trófica potencial desde un superdepredador hasta los productores primarios. La presencia de lince puede reducir la abundancia de carnívoros frugívoros e inducir cambios en sus patrones de alimentación que pueden modificar los patrones de dispersión de semillas con probables consecuencias para la demografía de muchas especies de plantas de fruto carnoso. Concluimos que el conocimiento de las interacciones ecológicas que componen las redes tróficas es esencial para diseñar estrategias de conservación eficaces, especialmente en programas de reintroducción.

A new large-scale index (AcED) for assessing traffic noise disturbance on wildlife: stress response in a roe deer (Capreolus capreolus) population.

Anthropogenic noise is a growing ubiquitous and pervasive pollutant as well as a recognised stressor that spreads throughout natural ecosystems. However, there is still an urgent need for the assessment of noise impact on natural ecosystems. This article presents a multidisciplinary study which made it possible to isolate noise due to road traffic to evaluate it as a major driver of detrimental effects on wildlife populations. A new indicator has been defined: AcED (the acoustic escape distance) and faecal cortisol metabolites (FCM) were extracted from roe deer faecal samples as a validated indicator of physiological stress in animals moving around in two low-traffic roads that cross a National Park in Spain. Two key findings turned out to be relevant in this study: (i) road identity (i.e. road type defined by traffic volume and average speed) and AcED were the variables that best explained the FCM values observed in roe deer, and (ii) FCM concentration was positively related to increasing traffic volume (road type) and AcED values. Our results suggest that FCM analysis and noise mapping have shown themselves to be useful tools in multidisciplinary approaches and environmental monitoring. Furthermore, our findings aroused the suspicion that low-traffic roads (< 1000 vehicles per day) could be capable of causing higher habitat degradation than has been deemed until now.

The seed dispersal syndrome hypothesis in ungulate-dominated landscapes.

The Seed Dispersal Syndrome Hypothesis (SDSH) posits that fruit traits predict the main dispersers interacting with plant species. Mammalian dispersers, relying heavily on olfactory cues, are expected to select dull-colored, scented, and larger fruits compared to birds. However, challenges like overabundant seed predators and context-dependency of frugivore-plant interactions complicate SDSH expectations. We studied the Iberian pear, Pyrus bourgaeana, an expected mammal-dispersed tree based on its fruit traits. Extensive camera-trapping data (over 35,000 records) from several tree populations and years revealed visits from seven frugivore groups, with ungulate fruit predators (59-97%) and carnivore seed dispersers (1-20%) most frequent, while birds, lagomorphs, and rodents were infrequent (0-10%). Red deer and wild boar were also the main fruit removers in all sites and years but acted as fruit and seed predators, and thus likely exert conflicting selection pressures to those exerted by seed dispersers. Although, as predicted by the SDSH, most Iberian pear fruits were consumed by large and medium-sized mammals, the traits of Iberian pear fruits likely reflect selection pressures from dispersal vectors in past times. Our results do not challenge the SDHS but do reveal the importance of considering frugivore functional roles for its adequate evaluation.

Top-down and bottom-up effects modulate species co-existence in a context of top predator restoration.

Mesopredators abundance is often limited by top-order predators and also by key food resources. However, the contribution of these bidirectional forces to structure carnivore community is still unclear. Here, we studied how the presence and absence of an apex predator which is currently recovering its former distribution range, the Iberian lynx (Lynx pardinus), determined the absolute abundance and fine-scale spatiotemporal avoidance mechanisms of two sympatric mesocarnivores (stone marten Martes foina and common genet Genetta genetta) with different dietary plasticity. We hypothesized that the lynx causes a mesopredator suppression and subordinate predators develop segregation strategies in respect to their trophic niche breadth. We placed 120 camera-traps in Southern Spain for 8 months in two consecutive years to estimate mesocarnivore abundances by using SCR Bayesian models, prey availability and assess spatio-temporal patterns. We found that the lynx reduced mesocarnivore abundance up to 10 times. Stone marten, a mesopredator with a broad food resources spectrum, showed a total spatial exclusion with the apex predator. Meanwhile, fine-scale avoidance mechanisms allowed the genet to persist in low density inside lynx territories, probably taking advantage of high availability of its preferred prey. Thus, the strength of these top-down and bottom-up effects was rather species-specific. Given the recent recovery of large carnivore populations worldwide, variation in suppression levels on different mesopredator species could modify ecosystem functions provided by the carnivore community in contrasting ways.

Conflicting selection on Cneorum tricoccon (Rutaceae) seed size caused by native and alien seed dispersers.

The disappearance of native seed dispersers due to anthropogenic activities is often accompanied by the introduction of alien species, which may to some extent replace the ecological service provided by the extinct ones. Yet, little empirical evidence exists demonstrating the evolutionary consequences of such alien "replacement." Here, we document the conflicting selection exerted on seed size by two native lizards (Podarcis lilfordi and P. pityusensis) and an alien mammal species (Martes martes), all acting as legitimate seed dispersers of the Mediterranean relict Cneorum tricoccon. While lizards mostly exerted a negative directional selection on seed diameter, especially P. pityusensis, the much larger pine marten exerted positive selection on seed size. Our findings suggest that this among-disperser variation in the selection regimes, together with the occurrence of spatial variation in the presence of each seed disperser, help to create the geographical variation observed for seed size of C. tricoccon. To our knowledge, this is the first empirical evidence showing opposing selective pressures between native and alien species in the seed dispersal process in an invaded ecosystem.

The effect of livestock on the physiological condition of roe deer (Capreolus capreolus) is modulated by habitat quality.

Free-range livestock grazing is a widespread human activity that not only modifies natural vegetation but also leads to interactions with wild ungulates. Most commonly, the interactions between cattle and wild ungulates have been studied with a focus on competition for high-quality forage. However, other mechanisms, such as the risk of parasite infection, might better describe this interaction. We aim to determine whether livestock affect roe deer (Capreolus capreolus Linnaeus, 1758) by reducing habitat quality and increasing the probability of infection by shared parasites. We measured noninvasive fecal cortisol metabolites as an indicator of habitat quality as well as the lung nematode larvae burden from the Dictyocaulus genus. A higher Dictyocaulus larvae load was found in the presence of livestock in pines, and feces collected in winter had a higher parasite load than feces collected in autumn. Additionally, fecal cortisol metabolite levels in the roe deer were affected by the interaction between habitat quality and livestock presence and were higher in the poorest habitat and when living in sympatry with cattle. Our results suggest that physiological stress responses in roe deer were mediated by the habitat type and the presence of competitors. The long-term implications of altered physiological responses such as those demonstrated here should be considered in management strategies for deer.

Spanish juniper gain expansion opportunities by counting on a functionally diverse dispersal assemblage community.

Seed dispersal is typically performed by a diverse array of species assemblages with different behavioral and morphological traits which determine dispersal quality (DQ, defined as the probability of recruitment of a dispersed seed). Fate of ecosystems to ongoing environmental changes is critically dependent on dispersal and mainly on DQ in novel scenarios. We assess here the DQ, thus the multiplicative effect of germination and survival probability to the first 3 years of life, for seeds dispersed by several bird species (Turdus spp.) and carnivores (Vulpes vulpes, Martes foina) in mature woodland remnants of Spanish juniper (Juniperus thurifera) and old fields which are being colonized by this species. Results showed that DQ was similar in mature woodlands and old fields. Germination rate for seeds dispersed by carnivores (11.5%) and thrushes (9.12%) was similar, however, interacted with microhabitat suitability. Seeds dispersed by carnivores reach the maximum germination rate on shrubs (16%), whereas seeds dispersed by thrushes did on female juniper canopies (15.5) indicating that each group of dispersers performed a directed dispersal. This directional effect was diluted when survival probability was considered: thrushes selected smaller seeds which had higher mortality in the seedling stage (70%) in relation to seedlings dispersed by carnivores (40%). Overall, thrushes resulted low-quality dispersers which provided a probability or recruitment of 2.5%, while a seed dispersed by carnivores had a probability of recruitment of 6.5%. Our findings show that generalist dispersers (i.e., carnivores) can provide a higher probability of recruitment than specialized dispersers (i.e., Turdus spp.). However, generalist species are usually opportunistic dispersers as their role as seed dispersers is dependent on the availability of trophic resources and species feeding preferences. As a result, J. thurifera dispersal community is composed by two functional groups of dispersers: specialized low-quality but trustworthy dispersers and generalist high-quality but opportunistic dispersers. The maintenance of both, generalist and specialist dispersers, in the dispersal assemblage community assures the dispersal services and increases the opportunities for regeneration and colonization of degraded areas under a land-use change scenario.

Colonization of abandoned land by Juniperus thurifera is mediated by the interaction of a diverse dispersal assemblage and environmental heterogeneity.

Land abandonment is one of the most powerful global change drivers in developed countries where recent rural exodus has been the norm. Abandonment of traditional land use practices has permitted the colonization of these areas by shrub and tree species. For fleshy fruited species the colonization of new areas is determined by the dispersal assemblage composition and abundance. In this study we showed how the relative contribution to the dispersal process by each animal species is modulated by the environmental heterogeneity and ecosystem structure. This complex interaction caused differential patterns on the seed dispersal in both, landscape patches in which the process of colonization is acting nowadays and mature woodlands of Juniperus thurifera, a relict tree distributed in the western Mediterranean Basin. Thrushes (Turdus spp) and carnivores (red fox and stone marten) dispersed a high amount of seeds while rabbits and sheeps only a tiny fraction. Thrushes dispersed a significant amount of seeds in new colonization areas, however they were limited by the presence of high perches with big crop size. While carnivores dispersed seeds to all studied habitats, even in those patches where no trees of J. thurifera were present, turning out to be critical for primary colonization. The presence of Pinus and Quercus was related to a reduced consumption of J. thurifera seeds while the presence of fleshy fruited shrubs was related with higher content of J. thurifera seeds in dispersers' faeces. Therefore environmental heterogeneity and ecosystem structure had a great influence on dispersers feeding behaviour, and should be considered in order to accurately describe the role of seed dispersal in ecological process, such as regeneration and colonization. J. thurifera expansion is not seed limited thanks to its diverse dispersal community, hence the conservation of all dispersers in an ecosystem enhance ecosystems services and resilience.