Mistletoes constitute instructive study cases with which to address the role of generalist consumers in the study of plant-animal interactions. Their ranges of safe sites for recruitment are among the most restricted of any plant; therefore, frugivores specializing in mistletoe have been considered almost indispensable for the seed dispersal of these parasitic plants. However, the absence of such specialists in numerous regions inhabited by many mistletoe species raises the question of whether unspecialized vectors may successfully disperse mistletoe seeds to narrowly defined safe sites. Using the European mistletoe Viscum album subsp. austriacum as a study case, we recorded a broad range of 11 bird species that disperse mistletoe seeds. For these species, we studied the mistletoe-visitation rate and feeding behavior to estimate the quantity component of dispersal effectiveness, and the post-foraging microhabitat use, seed handling, and recruitment probabilities of different microhabitats as a measure of the quality component of effectiveness. Both endozoochory and ectozoochory are valid dispersal mechanisms, as the seeds do not need to be ingested to germinate, increasing seed-dispersal versatility. Thrushes were the most effective dispersers, although they were rather inefficient, whereas small birds (both frugivores and non-frugivores) offered low-quantity but high-quality services for depositing seeds directly upon safe sites. As birds behave similarly on parasitized and non-parasitized hosts, and vectors have broad home ranges, reinfection within patches and the colonization of new patches are ensured by an ample assemblage of generalist birds. Thus, a parasitic plant requiring precision in seed dispersal can rely on unspecialized dispersers.
Summary Biota plays a central role as sources of spatial heterogeneity, having great potential to define ecological processes and patterns in the landscape. Mistletoes are fleshy‐fruited parasitic plants that dwell in forest canopies showing a strong aggregated spatial distribution. Parasitized trees potentially concentrate frugivore activity on their canopy, where birds find food, places to perch and protection against predators. Thus, seed‐deposition patterns generated from the canopy are expected to reflect the heterogeneity associated with the parasite. This becomes especially important in generalist dispersal systems; however, so far, we do not know the implications of mistletoe spatial heterogeneity on the seed‐dispersal pattern of other plants with which they simultaneously fruit. In a Mediterranean pineland, we analyse the impact of Viscum album subsp. austriacum on the seed‐deposition pattern of a zoochorous plant community, taking into consideration the spatial and temporal variability of environmental factors influencing the frugivore's habitat use, such as fruit availability and forest tree density. For four consecutive years, we studied 55 pairs of trees parasitized and unparasitized by mistletoe, analysing zoochorous fruit availability, frugivore visits and the zoochorous seed rain in selected trees. As expected, frugivorous birds responded to mistletoe heterogeneity by visiting parasitized trees preferentially to unparasitized ones, generating a differential deposition of mistletoe seeds on tree branches while dispersing seeds of co‐fruiting species under the host canopy. Availability of understory fruits remained similar in patches of parasitized and unparasitized trees, but showed strong temporal fluctuations reflected in the seed rain. On the other hand, mistletoe proved more copious in patches of parasitized trees and their fruit crops varied little between years, making mistletoes reliable food resources likely to lead to consistency in fruit‐deposition patterns. In conclusion, mistletoes, by patchily growing on the canopy layer and concentrating zoochorous seeds underneath, can shape the spatial seed‐deposition pattern of fleshy‐fruited plants in the forest. Moreover, as seeds constantly reach the same deposition sites over long periods, the soil beneath the host canopy could become hotspots for community regeneration. In degraded areas, such mistletoe effects might be critical, possibly promoting recolonization and vegetation recovery through the frugivore's activity.
Summary Parasitic plants are important drivers of community and ecosystem properties. In this study, we identify different mechanisms by which mistletoe (Viscum album subsp. austriacum) can affect soil chemical and biological properties at different temporal stages of parasitism. We quantified the effect of parasitism on host growth and the number of frugivorous mutualists visiting the host canopy. Then we collected, identified, and weighed the organic matter input underneath tree canopies and analyzed its nutrient content. Simultaneously, we analyzed soil samples under tree canopies and examined the chemical properties, microbial abundance, and functional evenness of heterotrophic microbial communities. Mistletoe increased the amount, quality, and diversity of organic matter input beneath the host canopy, directly through its nutrient‐rich litter and indirectly through a reduction in host litterfall and an increase in bird‐derived debris. All these effects gave rise to enriched hotspots able to support larger and more functionally even soil microbial communities beneath parasitized hosts, the effects of which were accentuated after host death. We conclude that mistletoe, together with the biotic interactions it mediates, plays a key role in intensifying soil resource availability, regulating the functional evenness, abundance, and spatial distribution of soil microbial communities.
• Premise of the study: Canopies are ecologically relevant compartments of forests. Multiple sources of heterogeneity interact within forest canopies due to their structural complexity, which exert major influences on the structure and composition of epiphyte communities. Here, we explore canopy environmental heterogeneity of a Mediterranean pine forest, identifying the key biotic and abiotic factors determining mistletoe (Viscum album subsp. austriacum) recruitment at coarse and fine spatial scales.• Methods: Through field experiments, we assessed the range of suitable host species for V. album subsp. austriacum (hereafter, V. a. austriacum). We characterized the variation in abiotic factors at a fine spatial scale on the host species. Finally, we examined the effects of biotic (predation) and abiotic (light, temperature) factors on the fate of mistletoe seeds and seedlings along host branches.• Key results: We confirmed the tight specificity of V. a. austriacum to pine species, in particular to P. nigra at the local scale. Biotic constraints increased toward the branch interior, with minor effects on apical locations due to the positive effect of pine-needle coverage. Contrarily, abiotic constraints increased toward branch extremities, harming mistletoe seeds by encouraging their desiccation.• Conclusions: Biotic and abiotic variables exert a strong, nonrandom filter on V. album regeneration, resulting in recruitment hotspots at the periphery of the branches and sites with a high probability of recruitment failure at thicker and more exposed locations. The narrow range of suitable host species and the scarcity and spatially restricted recruitment hotspots for V. a. austriacum leads to the clumping of mistletoe populations at the finer spatial scale.
Climate change will alter the biotic and abiotic environment and dissipate ecological barriers, reorganising maps of current distribution of parasites and their hosts. In this study, we analyse the population dynamics of the parasitic plant Viscum album subsp. austriacum and explore key biotic (host availability and seed dispersal) as well as abiotic (temperature) factors influencing elevational distribution. The study was conducted along an elevational gradient of a Mediterranean mountain, covering the distribution belts of three potential pine hosts: Pinus halepensis (1300–1500 m), P. nigra (1300–1900 m) and P. sylvestris var. nevadensis (1600–2000 m). Along this gradient, we measured multiple variables of mistletoe population (prevalence, abundance and demographic profile) and different factors that might define the current mistletoe distribution (host suitability and availability, temperature and seed dispersal services). We found a decline in mistletoe prevalence and abundance with increasing elevation, detecting larger values of both variables at lower elevations of the most suitable host (Pinus nigra). Pinus sylvestris var. nevadensis was a suboptimal but suitable host for the parasite at high elevations. Mistletoe found suitable temperatures and seed dispersal services all along the gradient, being able to recruit at any site. With warming temperatures, the presence of suitable vectors for parasite dispersion, and the presence of a sub‐optimal host (P. sylvestris var. nevadensis) at the mountain top, mistletoe currently has a window of opportunity to expand its present geographic distribution to the summits.
The capacity of parasitic plants in structuring natural communities is increasingly recognized. These plants can affect the structure, composition and productivity of plant communities by modifying the competitive balance between hosts and non‐host species and by altering the quantity and quality of resources entering the soil. Despite the progress made in this field, there is still a lack of integrative studies showing the structuring capacity of parasitic plants in forest ecosystems, where their effect may be less detectable due to the long life span of the system. In this study we evaluate the long‐term impact of Viscum album subsp. austriacum on the woody‐plant community of a Mediterranean pineland. This mistletoe remains several years on the same host, exerting long‐lasting, spatially concentrated effects on community and ecosystem characteristics. Mistletoe concentrates zoochorous seeds and induces changes in the soil fertility and light availability beneath the canopy of parasitized trees, which have the potential to facilitate zoochorous–plant colonization, recruitment, and growth at the same time as it weakens the host. Here, we analyse whether mistletoe‐driven changes could result in a nucleus of zoochorous woody plants nourished by the abundant organic detritus accumulated under the host. We also analyse whether mistletoe effects can expand after host death. We selected unparasitized, parasitized, and dead parasitized Pinus nigra trees, in which we studied the joint effect of mistletoe‐mediated changes in soil nutrient and light availability, with the seed rain, seed predation, seedling establishment, plant recruitment, and plant growth. Light‐ and soil‐nutrient resources were greater under parasitized trees, and intensified after host death. The seed rain was maximum under parasitized trees, where seedling recruitment proved more likely. Sapling density, richness, and growth increased with the development of parasitism. Our findings show that V. album exerts a strong and lasting impact on the structure and dynamics of Mediterranean pinelands, with parasitized trees acting as centres for the establishment and growth of colonizing fleshy‐fruited woody species, which, over the long term, promote vegetation shifts by limiting dominant pine trees and facilitating less represented fleshy‐fruited shrubs. A http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.12907/suppinfo is available for this article.
Parasitic plants, among many other parasitic organisms, are shifting in their geographic distribution in response to global change, establishing novel interactions with susceptible but previously unexposed host plants. Projections of future species assemblages in increasingly changing environments frequently overlook the strong capacity of these parasites to transform ecological systems, and host switching is considered a mere change of partner with no subsequent impact on ecosystem properties. We explore the ecological consequences of parasite host shifts analysing the growth and reproductive responses of two host trees that share a different interaction‐history with the parasitic plant Viscum album: recent in the case of Pinus sylvestris subsp. nevadensis and longstanding in that of Pinus nigra. We quantified growth by measuring primary (bud elongation) and secondary (dendrochronology) tree growth, and reproduction by quantifying cone crops, cone size, seed production, seed weight, seed germination, and emergence success. Pinus nigra registered a minor effect on reproduction but a major reduction in biomass, clearly reflected in lower primary and secondary tree growth, smaller cones and lighter seeds. On the contrary, P. sylvestris subsp. nevadensis underwent a strong decline of its reproductive capacity with no effects on growth, manifested in smaller cone crops, less seed production, and lower germination and emergence success. Synthesis. Mistletoe parasitism unleashes contrasting responses in taxonomically close host species with sharply different consequences for the forest ecosystem. While old hosts tolerate better the effect of parasitism, minimizing the impact on reproduction at the expense of their growth, recent hosts undergo greater effects of parasitism, suffering reproductive collapse with no perceptible loss of growth. We conclude that the increasing phenomenon of parasite host switching is not just a mere change of partner, but a driver of a new ecosystem organization. These results highlight the importance of considering the specific effects of newly established interactions when predicting future species assemblages, as these can trigger different ecological organizations from those we currently know.
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