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.
Resumen
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.
Red fox (Vulpes vulpes) foraging placidly on Iberian pear fruits (Pyrus bourgaeana) in one fruit depot created for the field experiment of this study outside Iberian lynx (Lynx pardinus) ranges.
Agricultural intensification, afforestation and land abandonment are major drivers of biodiversity loss in semi‐natural grasslands across Europe. Reversing these losses requires the reinstatement of ...plant–animal interactions such as pollination. Here we assessed the differences in species composition and patterns of plant‐pollinator interactions in ancient and restored grasslands and how these patterns are influenced by landscape connectivity, across three European regions (Belgium, Germany and Sweden).
We evaluated the differences in pollinator community assemblage, abundance and interaction network structure between 24 ancient and restored grasslands. We then assessed the effect of surrounding landscape functional connectivity (i.e. green infrastructure, GI) on these variables and tested possible consequences on the reproduction of two model plants, Lotus corniculatus and Salvia pratensis.
Neither pollinator richness nor species composition differed between ancient and restored grasslands. A high turnover of interactions across grasslands was detected but was mainly due to replacement of pollinator and plant species. The impact of grassland restoration was consistent across various pollinator functional groups, whereas the surrounding GI had differential effects. Notably, bees, butterflies, beetles, and dipterans (excluding hoverflies) exhibited the most significant responses to GI variations. Interestingly, networks in restored grasslands were more specialised (i.e. less functionally redundant) than in ancient ones and also showed a higher number of insect visits to habitat‐generalist plant species. Landscape connectivity had a similar effect, with habitat‐specialist plant species receiving fewer visits at higher GI values.
Fruit set in S. pratensis and L. corniculatus was unaffected by grassland type or GI. However, the fruit set in the specialist S. pratensis increased with the number of pollinator visits, indicating a positive correlation between pollinator activity and reproductive success in this particular species.
Synthesis and applications. Our findings provide evidence of the necessity to enhance ecosystem functions while avoiding biotic homogenisation. Restoration programs should aim at increasing landscape connectivity which influences plant communities, pollinator assemblages and their interaction patterns. To avoid generalist species taking over from specialists in restored grasslands, we suggest reinforcing the presence of specialist species in the latter, for instance by means of introductions, as well as increasing the connectivity to source populations.
Resumen
La intensificación agrícola, la forestación y el abandono de tierras son factores clave en la pérdida de biodiversidad en pastizales semi‐naturales en toda Europa. Revertir estas pérdidas requiere restablecer interacciones planta‐animal, como la polinización. En este estudio, evaluamos las diferencias en la composición de especies y patrones de interacciones planta‐polinizador en pastizales antiguos y restaurados, y cómo estos patrones son influenciados por la conectividad del paisaje en tres regiones europeas (Bélgica, Alemania y Suecia).
Examinamos las diferencias en el ensamblaje de la comunidad de polinizadores, su abundancia y la estructura de la red de interacciones planta‐polinizador en 24 pastizales antiguos y restaurados. Luego, evaluamos el efecto de la conectividad funcional del paisaje circundante (es decir, infraestructura verde, GI) en estas variables y evaluamos posibles consecuencias en la reproducción de dos plantas modelo, Lotus corniculatus y Salvia pratensis.
No hubo diferencias en la riqueza de polinizadores ni en la composición de especies entre los pastizales antiguos y restaurados. El impacto de la restauración de pastizales fue consistente en diversos grupos funcionales de polinizadores, mientras que la GI circundante tuvo efectos diferenciales. Destacadamente, abejas, mariposas, escarabajos y dípteros (excluyendo sírfidos) mostraron las respuestas más significativas a las variaciones en la GI. Curiosamente, las redes en pastizales restaurados fueron más especializadas (menos funcionalmente redundantes) que en los antiguos y también mostraron un mayor número de visitas de insectos a especies de plantas generalistas de hábitat. La conectividad del paisaje tuvo un efecto similar, con especies de plantas especializadas recibiendo menos visitas a mayores valores de GI.
La producción de frutos en S. pratensis y L. corniculatus no se vió afectada por el tipo de pastizal o la GI. Sin embargo, la producción de frutos en la especialista S. pratensis aumentó con el número de visitas de polinizadores, indicando una correlación positiva entre la actividad de polinización y el éxito reproductivo en esta especie.
Síntesis y aplicaciones. Nuestros resultados evidencian la necesidad de evitar la homogeneización biótica. Los programas de restauración deben apuntar a aumentar la conectividad del paisaje, que influye en las comunidades de plantas y polinizadores y sus patrones de interacción. Para evitar que especies generalistas desplacen a especialistas en pastizales restaurados, sugerimos reforzar la presencia de especies especialistas en estos, por ejemplo, mediante introducciones, así como aumentar la conectividad con poblaciones fuente.
Our findings provide evidence of the necessity to enhance ecosystem functions while avoiding biotic homogenisation. Restoration programs should aim at increasing landscape connectivity which influences plant communities, pollinator assemblages and their interaction patterns. To avoid generalist species taking over from specialists in restored grasslands, we suggest reinforcing the presence of specialist species in the latter, for instance by means of introductions, as well as increasing the connectivity to source populations.
Current global change scenarios demand knowledge on how anthropogenic impacts affect ecosystem functioning through changes in food web structure. Frugivorous mesocarnivores are a key link in trophic ...cascades because, while their abundance and behaviour are usually controlled by apex predators, they can provide high‐quality seed‐dispersal services to plant communities. Thus, the recent rewilding of large carnivores worldwide can trigger cascading effects for plants.
We investigated the top‐down effects of an apex predator (Iberian lynx Lynx pardinus) on seed‐dispersal services mediated by two mesocarnivore species (red fox Vulpes vulpes and stone marten Martes foina) at the plant community level by comparing areas with and without lynx in a Mediterranean mountain range in Southern Spain.
We collected scats of mesocarnivores (n = 1575) to assess frugivory and seed dispersal of 15 plant species over two consecutive fruiting seasons and two habitat types (open and forest). Specifically, we assessed the effect of lynx presence on (i) seed occurrence and fleshy‐fruit biomass per scat, (ii) number of scats containing seeds and (iii) diversity of dispersed seeds.
The quantity and diversity of dispersed seeds drastically decreased under predation risk for both mesocarnivore's species. Seed dispersal by stone martens was negatively affected by the presence of lynx, with a marked reduction in the number of scats with seeds (93%) and the diversity of dispersed seeds (46%). Foxes dispersed 68% fewer seeds in open habitats when coexisting with lynx, probably leading to differential contributions to seed‐dispersal effectiveness among habitats.
Our study reveals a novel trophic cascade from apex predators to plant communities. The behavioural responses of frugivorous mesocarnivores to predation risk and the reduction in the intensity of their faecal deposition pattern are probably related to their lower abundance when co‐occurring with apex predators. While rewilding apex predators is a successful conservation tool, attention should be paid to cascading effects across food webs, particularly where frugivore megafauna is missing and mesocarnivores provide unique services to plants.
Read the free Plain Language Summary for this article on the Journal blog.
Resumen
El escenario actual de cambio global demanda más conocimiento sobre cómo los impactos antrópicos afectan al funcionamiento de los ecosistemas a través de cambios en la estructura de la red trófica. Los mesocarnívoros frugívoros son un eslabón clave en las cascadas tróficas ya que, si bien su abundancia y comportamiento suelen estar controlados por los superdepredadores, pueden proporcionar servicios de dispersión de semillas de alta calidad a las comunidades de plantas. Así, la reciente recuperación de grandes carnívoros en todo el mundo puede desencadenar efectos en cascada para las plantas.
Investigamos los efectos en cascada de un superdepredador (lince ibérico Lynx pardinus) sobre los servicios de dispersión de semillas mediados por dos especies mesocarnívoras (zorro rojo Vulpes vulpes y garduña Martes foina) a nivel de toda la comunidad de plantas y comparando áreas con y sin lince en las montañas mediterráneas del sur de España.
Recolectamos excrementos de mesocarnívoros (n = 1575) para evaluar la frugivoría y la dispersión de semillas de 15 especies de plantas durante dos temporadas de fructificación consecutivas y en dos tipos de hábitat (abierto y forestal). Específicamente, evaluamos el efecto de la presencia de linces sobre (i) la presencia de semillas y la biomasa de frutos por excremento, (ii) el número de excrementos que contenían semillas y (iii) la diversidad de semillas dispersadas.
La cantidad y diversidad de semillas dispersadas disminuyeron drásticamente bajo el escenario de riesgo de depredación para ambas especies de mesocarnívoros. La dispersión de semillas por las garduñas se vio afectada negativamente por la presencia del lince, con una marcada reducción en el número de excrementos con semillas (93%) y la diversidad de semillas dispersadas (46%). Los zorros dispersaron un 68% menos semillas en hábitats abiertos cuando coexistieron con el lince, lo que probablemente condujo a una contribución diferente en la efectividad de la dispersión de semillas entre hábitats.
Nuestro estudio revela una nueva cascada trófica desde los superdepredadores hasta las comunidades de plantas. Las respuestas comportamentales de los mesocarnívoros frugívoros al riesgo de depredación y la reducción de sus patrones de marcaje fecal probablemente estén relacionados con su menor abundancia cuando coexisten con los superdepredadores. Aunque la recuperación de los superdepredadores es una herramienta de conservación exitosa, se debe prestar atención a sus efectos en cascada en las redes tróficas, particularmente en escenarios donde la megafauna frugívora ha desaparecido y los mesocarnívoros brindan servicios únicos a las comunidades de plantas.
Read the free Plain Language Summary for this article on the Journal blog.
Spatial patterns of plant species are determined by an array of ecologica factors including biotic and abiotic environmental constraints and intrinsic species traits. Thus, an observed aggregated ...pattern may be the result of short-distance dispersal, the presence of habitat heterogeneity, plant–plant interactions or a combination of the above. Here, we studied the spatial pattern of Mediterranean alpine plant Silene ciliata (Caryophyllaceae) in five populations and assessed the contribution of dispersal, habitat heterogeneity and conspecific plant interactions to observed patterns. For this purpose, we used spatial point pattern analysis combined with specific a priori hypotheses linked to spatial pattern creation. The spatial pattern of S. ciliata recruits was not homogeneous and showed small-scale aggregation. This is consistent with the species’ shortdistance seed dispersal and the heterogeneous distribution of suitable sites for germination and establishment. Furthermore, the spatial pattern of recruits was independent of the spatial pattern of adults. This suggests a low relevance of adultrecruits interactions in the spatial pattern creation. The difference in aggregation between recruits and adults suggests that once established, recruits are subjected to self-thinning. However, seedling mortality did not erase the spatial pattern generated by seed dispersal, as S. ciliata adults were still aggregated. Thus, the spatial aggregation of adults is probably due to seed dispersal limitation and the heterogeneous distribution of suitable sites at seedling establishment rather than the presence of positive plant–plant interactions at the adult stage. In fact, a negative density-dependent effect of the conspecific neighbourhood was found on adult reproductive performance. Overall, results provide empirical evidence of the lack of a simple and direct relationship between the spatial structure of plant populations and the sign of plant–plant interactions and outline the importance of considering dispersal and habitat heterogeneity when performing spatial analysis assessments.
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.
Generalist seed dispersers such as carnivores provided more probability of recruitment than specialized dispersers (Turdus spp.) on woodlands and old fields recently colonized.
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 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.
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.
Climate change is forcing the redistribution of life on Earth at an unprecedented velocity
. Migratory birds are thought to help plants to track climate change through long-distance seed dispersal
. ...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.
PDF
