Research articleEffects of habitat fragmentation on frugivorous birds and on seed removal from Pistacia lentiscus in two contrasting fruiting seasons
Introduction
Seed dispersal is a key step in the life cycle of plants as it provides an independent dispersal phase for a new and genetically distinctive individual that can potentially colonize and establish itself in novel environments (Jordano, 2017). Consequently, seed dispersal is a determinant factor in the structure and dynamics of plant populations and communities (Janzen, 1970). In animal seed-dispersed plants, frugivores either regurgitate or defecate undamaged seeds away from parent plants (Jordano, 2000). The probability of seed removal and the patterns of seed dispersal are thus strongly influenced by spatial environmental factors affecting frugivore abundance and behavior such as food availability, the heterogeneity of microhabitat in terms of shelter and breeding sites, and the functional connectivity between habitats (Corrêa Côrtes and Uriarte, 2012). However, current changes in landscape configuration due to human activities leading to forest loss and fragmentation may alter the abundance of both fruiting plants and frugivores (Stiles, 1980; Restrepo and Gomez, 1998; Restrepo et al., 1999).
Habitat loss and fragmentation change the original spatial structure of the landscape by reducing the size and connectivity of remaining habitat fragments, which will probably affect the mutualistic interactions of animal seed dispersal (Emer et al., 2018). One key aspect to consider when assessing the effects of fragmentation on plant–animal seed dispersal is the relative mobility of the seed disperser. For example, habitat fragmentation can alter the distribution of certain frugivorous species with low mobility that are restricted to specific environments, while other frugivores with greater mobility may be capable of using a non-forested matrix and thus be able to increase their abundance in moderately marginalized fragmented habitats (Farwig et al., 2006). Furthermore, habitat fragmentation may change the composition of the disperser guild by reducing the abundance of large-bodied avian dispersers, thereby decreasing the probability that long-distance dispersal events from small habitat fragments will take place (Uriarte et al., 2011). Generally, large frugivores will have stricter feeding and habitat requirements than smaller ones, which are able to live in small and low-quality forest fragments (Uriarte et al., 2011).
However, not all frugivorous birds establish mutualistic interactions and disperse seeds. Some species act as antagonists since they eat the seeds (e.g. granivorous birds) and kill the embryo, thereby reducing female plant fitness (Verdú and García-Fayos, 2001). Habitat fragmentation may also affect seed removal by modifying the behavior of animal dispersers (Herrera, 1995), thereby altering the balance between mutualistic and antagonistic interactions (Jules and Rathcke, 1999; Herrera et al., 2011). A shift toward more antagonistic interactions (e.g. seed predation) and less seed removal will harm forest regeneration dynamics (Neuschulz et al., 2016). At the end of the fruiting period the plant will have interacted with both dispersers and predators and the relative balance between them will determine the net amount of seed dispersal. In the long term, habitat fragmentation may change the regenerative potential of plant species by affecting the recruitment and regeneration of plant populations (García et al., 2012; Rey and Alcántara, 2013).
Additionally, seed dispersal mediated by animal vectors is strongly influenced by seasonal variation in fruit production. This is the case of masting behavior (i.e. the annual variation in fruit production) in certain plant species that represent key fruit resources for frugivorous birds. Similarly, masting can reduce seed predation by satiating predators through an abundance of available fruit and, consequently, may improve plant fitness (Mezquida and Olano, 2013). Masting can affect the presence and abundance of frugivorous birds in forests and therefore plant–frugivore interactions (Jordano, 1985). Movements by frugivorous animals may in fact reflect the underlying seasonal variability in the availability of fruit resources rather than the nature of the habitat cover itself (Lehouck et al., 2009; Herrera and García, 2010; Herrera et al., 2011). Despite the importance of seasonal variation imposed by masting, to date only a few studies spanning a temporal window of more than a single season have ever been published (e.g. Jordano, 1987; Alcántara et al., 1997; Herrera and García, 2009; Herrera et al., 2011).
Seed removal by animals is also affected by spatial variation in microhabitat heterogeneity. This process frequently exhibits non-random patterns biased toward certain microhabitats within the landscape (Schupp et al., 2002). Consequently, frugivores may disperse seeds unevenly by occupying preferred microhabitats, which will create contagious spatial distributions of dispersed seeds (Schupp et al., 2002). Ultimately, a nucleation process of this nature affects seed survival and seedling establishment, as well, subsequently, as the structure and dynamics of plant populations and communities (Howe and Smallwood, 1982; Wang and Smith, 2002; Nathan, 2006; Clark et al., 2007; González-Castro et al., 2015).
In this study, we evaluated the effects of habitat fragmentation on the seed dispersers and seed predators of the Mediterranean masting species Pistacia lentiscus L. (Anacardiaceae) in two contrasting fruiting seasons (high and low production). More specifically, we (i) compared the abundance and composition of the avian frugivores, (ii) recorded fruit-removal rates by fruit dispersers and predators, and (iii) investigated potential changes in the final destination of seeds. We expected to find greater frugivore richness and abundance in connected than in physically isolated forest fragments. In addition, we expected small-sized frugivorous bird species to dominate in the frugivore guild in connected forest fragments, but that medium-sized birds would occur in both isolated and connected forest fragments (Uriarte et al., 2011). Furthermore, since P. lentiscus is a masting species, we hypothesized that there would be greater dispersal and predation rates during a high fruit production season (the mast season, hereafter), and that interactions would be similar in both connected and isolated forest fragments during the mast season. Finally, because frugivorous birds visit female plants for longer and regurgitate or defecate the seeds in the same place as they ingest them, we expected higher levels of seed dispersal under female Pistacia plants than in other microhabitat types (Verdú and García-Fayos, 2002; González-Varo et al., 2018).
Section snippets
Study species
Pistacia lentiscus is a common evergreen sclerophyllous shrub of up to 3–5 m in height, widely distributed throughout the Mediterranean region. It is dioecious and wind-pollinated; its fruit consist of one-seeded drupes that ripen in September–March (Verdú and García-Fayos, 1998). Fruit ripening is associated with a change of color from white to red and then to black. Black fruits are most likely to bear a viable seed, while red and white fruits are either deceptive fruits of parthenocarpic
Results
As expected, initial fruit availability differed between seasons (Tables 1 and S2, Fig. 2a). During the mast season P. lentiscus yielded a large crop and was basically the only species with fleshy fruit in the study fragments. The estimated mean (± SD) fruit production of P. lentiscus plants during the mast season was 62,150 fruit per individual (51,650 and 72,650 in connected and isolated fragments, respectively). By contrast, during the non-mast season fruit production dropped dramatically to
Discussion
In this study we found a greater abundance of seed dispersers in connected than in isolated forest fragments during the mast season but the opposite pattern in the non-mast season. However, small seed dispersers, which are responsible for most dispersal events, showed no differences in abundance. We detected a higher abundance of seed predators in isolated fragments and thus we would have expected to find lower rates of seed removal by legitimate seed dispersers in isolated fragmented forests
Acknowledgements
We would like to thank the local landowners for permission to work at the study sites, Lorena Ashworth, Ana Calviño and Pedro Jordano for valuable comments, Encarnación Rubio-Perez for field and laboratory assistance, and Michael Lockwood for the linguistic correction. This study was supported by a grant from the Spanish Ministry of Economy and Competitiveness (CGL2011- 23721). CPF is supported by a predoctoral fellowship from Ministry of Economy and Competitiveness (BES-2012-055103), research
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Current address: Mediterranean Institute for Agriculture, Environment and Development (MED), University of Évora, Casa Cordovil 7000–651, Évora, Portugal.