Ecological interactions mediated by the european mistletoe, viscum album subsp. Austriacum, in mediterranean forests—an integrated perspective

  1. Mellado García, Ana
Dirigida por:
  1. Regino Zamora Director

Universidad de defensa: Universidad de Granada

Fecha de defensa: 02 de marzo de 2016

Tribunal:
  1. Pedro José Rey Zamora Presidente/a
  2. José Antonio Hódar Correa Secretario
  3. Miguel Verdú del Campo Vocal
  4. José M. Gómez Reyes Vocal
  5. Susana Rodríguez Echeverría Vocal
Departamento:
  1. ECOLOGÍA

Tipo: Tesis

Resumen

In this thesis, we seek a deeper and broader understanding of the ecological interactions mediated by the mistletoe Viscum album subsp. austriacum in Mediterranean forests. Mistletoes constitute an interesting group of hemiparasitic epiphytes widely distributed around the world that have been thoroughly investigated with respect to their physiology, morphology, pharmacology and their role as forest pest. However, many aspects of their ecology remains a mystery. Better known as harmful parasites that decrease the vigor of their host trees, today we have little knowledge about the ecological interactions mediated by these parasites, as well as their direct and indirect effects on natural communities and ecosystems. In this thesis, we show that, although being a minor component of the forest community (in terms of abundance and biomass), mistletoe can play a relevant role in the forest. Besides its detrimental effect on the host, mistletoe parasitism promotes a series of direct and indirect effects able to affect the structure and dynamic of the forest community, as well as key ecosystem processes, such as nutrient cycling. Spread over five chapters we study the close relationship of mistletoe with its host trees and seed dispersers, as well as the effect of the parasite on different organisms of the natural community and ecosystem properties. In Chapter I, we focus on the mistletoe-host interaction. We analyze different factors shaping the spatial distribution of Viscum a. austriacum in the forest canopy, including the host specificity and the variation of biotic and abiotic factors limiting safe sites for mistletoe recruitment. We found that mistletoe shows a strong host specificity for pine species, in particular for Pinus nigra (the most abundant species) at the local scale. We also found that biotic (seed predation) and abiotic (light and temperature) factors exert a non-random filter on mistletoe regeneration, resulting in recruitment hotspots at the periphery of tree branches, under pine-needle protection, and sites with high probability of recruitment failure at thicker and more exposed locations. In Chapter II, we focus on the mistletoe-vector interaction. We study the seed dispersal effectiveness of an unspecialized group of frugivorous birds providing dispersal services to a parasitic plant with extremely narrow ranges of safe sites to recruit. Our results indicate that a wide and heterogeneous assemblage of generalist birds successfully disperse mistletoe seeds by two different mechanisms: endozoochory and ectozoochory. Large generalist birds (Thrushes) constitute the most effective dispersal group; however, they provide low-efficiency services, consuming numerous fruits in order to successfully disperse a single seed. In contrast, small generalist birds provide better quality and more efficient dispersal, but of low-quantity. Finally, opportunistic birds are very efficient dispersers by moving seeds externally and directly to safe sites of the tree periphery. By having a wide and heterogeneous range of seed dispersers mistletoe ensures the maintenance of re-infection processes within the population and the colonization of new infection foci. In Chapter III, we examine interactions between mistletoe and fleshy-fruited plants of the understory. We analyze the effect of Viscum a. austriacum spatial heterogeneity on the seed-deposition pattern of the zoochorous plant community. We observed that frugivorous birds respond to mistletoe patchiness by visiting parasitized trees preferentially to unparasitized ones, generating a differential deposition of mistletoe seeds on tree branches, increasing re-infection processes within the host, while dispersing seeds of co-fruiting species under the host canopy. Moreover, as mistletoe fruit-crops vary little from one year to the next, there is a temporal persistency of seed deposition sites, with the canopy of parasitized trees consistently receiving large mistletoe seed rain. Otherwise, understory species show strong fruit-crop fluctuations between different years, which is reflected in the abundance of seeds reaching microsites beneath the host each year. In Chapter IV, we explore mistletoe-mediated aboveground-belowground interactions. We analyze the effect of Viscum a. austriacum and the parasitic and mutualistic interactions it mediates from the forest canopy on soil-chemical and biological properties. We found that mistletoe modifies the linkages between the forest canopy and the soil through time, increasing the amount, quality and diversity of organic matter inputs beneath the host canopy, directly through its nutrient-rich litter and indirectly through the decrease of host litterfall and the increase of bird-derived debris. This greater abundance and diversity of organic compounds gives rise to enriched hotspots able to support greater and more functionally diverse soil microbial communities beneath parasitized hosts, the effects of which are accentuated after host death. Thus, mistletoe, enhanced by the biotic interactions it mediates, intensifies soil-resource availability, regulating composition, abundance and spatial distribution of soil microbial communities. In Chapter V, we study the effect of mistletoe on the structure and dynamics of the plant community. We seek to understand whether mistletoe-induced changes under host patches, coupled to the effect of post-dispersal processes, ultimately result in changes in the plant community assemblage. We found that Viscum a. austriacum plays an important role in structuring the plant community. Mistletoe induces significant changes on host growth through its parasitic interaction, leading to greater light infiltration to the forest floor. At the same time, mistletoe facilitates seed arrival of understory species on the fertilization islands generated beneath the host, where conditions for seedling establishment improve. Consequently, parasitized trees concentrate a more abundant and richer fleshy-fruited plant assemblage than non-parasitized trees, and, in turn, enhance plant growth. Moreover, by coupling detrimental effects on their hosts and facilitative effects on the woody-plant community over long time periods, mistletoe affects patch dynamics and community succession, promoting the replacement of a dominant host tree (Pinus nigra) by a diverse community of subdominant zoochorous plants. In conclusion, by taking a broader view of mistletoe and considering a wider breadth of its biotic interactions, we found several direct and indirect facilitative effects of the parasite on different organisms in the community. On the one hand, mistletoe induces significant changes on the growth of the dominant tree through its parasitic interaction, while facilitating colonization and establishment of less represented species (zoochorous-shrub species), leading to changes in the configuration of the plant community. On the other hand, through modified organic matter input to the soil and affecting belowground processes, mistletoe exerts facilitative effects on soil microbial communities and also enhances the growth of understory shrubs. Thus, far from being a harmful organism, our findings show that mistletoe can play an important role in regulating the spatial-temporal dynamic of the forest ecosystem, enhancing the structural and biological complexity of the forest its inhabits.