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«Dissertation In partial fulfilment of the requirements for the award of a Doctorate Degree in Natural Sciences (Dr. rer. nat) The Faculty of Biology, ...»

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Plant-frugivore interactions in a heterogeneous

forest landscape of South Africa


In partial fulfilment of the requirements

for the award of a

Doctorate Degree in Natural Sciences (Dr. rer. nat)

The Faculty of Biology, Philipps-University of Marburg

Lackson Chama, MSc

Sinazongwe (Zambia)

June 2012, Marburg

From the Faculty of Biology, Philipps-University Marburg

als Dissertation am angenommen.

Dekan: Prof. Dr. Paul Galland Erstgutachterin: Prof. Dr. N. Farwig Zweitgutachter: Prof. Dr. R. Brandl 25th June 2012

Tag der Disputation:

Dedicated to my son, Mishila, who’s first two years on earth I was hardly part of, due to my commitment towards this work.










































APPENDIX B …………………………………………………………………………………………………………………………………..……… 83 APPENDIX C





Chapter 1: General Introduction Effects of human activities on forest biodiversity Human-driven activities constitute the most serious threat linked with the loss of Earth's biological diversity (Forman & Collinge 1996, Bergman et al. 2004, Gibson et al. 2011). A recent global assessment of the impacts of human disturbance on biodiversity by Gibson et al. (2011) suggests that these threats are particularly high in tropical forest landscapes where both species diversity and human pressures on natural environments are high. The rapid increase in human land-use activities involving the conversion of tropical forests for agriculture and timber production (FAO 2006, Gibson et al. 2011) has not only considerably reduced the sizes of remaining forest, but also disproportionally increased the size of human dominated matrix surrounding these forest patches (Debinski & Holt 2000, Fahrig 2003). This leads to increased forest isolation and can undermine the quality of forest habitats (Saunders et al. 1991, Wunderle 1997, Fischer & Lindenmayer 2007).

Moreover, these changes can alter the physical space where species grow and interact, and thus trigger biological responses that may lead to the disruption of species composition (Montoya 2008). With the global human population predicted to grow even further in the next three decades, it looks likely that these human driven threats on biodiversity will equally increase (Primack 2002) and could adversely impact on key ecological processes such as seed dispersal.

The process of seed dispersal plays a pivotal role in the regeneration and restoration of plant communities across forest ecosystems globally (Howe & Smallwood 1982). For instance, up to 50 and 90% of fleshy fruiting plant species in temperate and tropical forest ecosystems, respectively, depend on this process for the transportation of their propagules to suitable habitats (Aizen et al. 2002, Herrera 2003). Several studies showed that both forest patch quality and matrix habitat can modify single-pair seed dispersal interactions. However, these interactions have been shown to be linked in complex networks of mutually dependent plants and frugivores species (Fortuna & Bascompte 2006, Bascompte & Jordano 2007). Here, studies so far are scare. With human activities increasingly likely to further isolate and reduce the sizes and quality of remaining forest patches (Rosenberg et al. 1999), it is vital to study plant-frugivore interactions in a community approach to better understand the effects of habitat modification on seed dispersal processes. Further, the functional roles in terms of species contribution and traits should be considered.

Plant-frugivore interactions in changing landscapes

Plant-frugivore mutualistic interactions form the physical template for seed dispersal and thus forest regeneration (Bascompte & Jordano 2007). Recent studies have shown that these interactions are often assembled in form of complex networks of interdependencies between species of both plants and frugivores (Bascompte & Jordano 2007, Reid & Armesto 2011, Menke et al. 2012). The pattern of interactions in the networks is highly heterogeneous, suggesting that a large proportion of species have less and weak interactions, while a few are much more connected than expected by chance (Fortuna & Bascompte 2006, Vázquez et al. 2009). This result in the formation of a nested plant-frugivore community, where less connected species interacts with a subset of the most connected species (Bascompte et al. 2003, Bascompte & Jordano 2007). These community structures can have important implications for the stability of plant-frugivore interactions especially in the face of human triggered habitat fragmentation (Fortuna & Bascompte 2006, Tylianakis et al. 2010a). However, not many studies have considered the effects of habitat fragmentation on seed dispersal networks.

So far it is known that species react differently to habitat modification due to different sensitivity to disturbances (Watson et al. 2005, Van Houtan et al. 2007). For instance, while some species may be able to take advantage of new ‘habitats’ provided by intervening matrix, such as farmland or scattered trees within farmland, others may not (Andren 1994). These changes in forest landscapes can lead to the decline and loss of key dispersers which may alter the interaction structure in mutualistic networks (Cordeiro & Howe 2003, Kirika et al. 2008). Thus, examining complex plant-frugivore mutualistic networks can help to better understand the long-term effects of anthropogenic impacts on the processes of seed dispersal (Bascompte & Jordano 2007). The functional diversity of frugivores within these communities should also be considered as this might save as a suitable indicator of network stability to habitat modification, than the network structure per se.

The role of functional diversity in frugivore communities

Functional diversity defines the variety and significance of species traits that drives and sustains the functioning of an ecosystem (Naeem et al. 2000, Tilman 2001, Cadotte et al. 2011). In the case of frugivorous birds, functional diversity is determined by traits related to seed dispersal, such as body mass, gape width and relative dietary dominance by fruit or feeding behavior (Fleming et al.

1993, Dennis & Westcott 2006). For example, larger frugivores may have the ability to consume large proportions of fruit, retain them for much longer in their digestive tracts and transport them over longer distances than smaller birds (Spiegel & Nathan 2007). Moreover, frugivores have generally also been shown to have different degrees of frugivory, whereby some species will almost entirely depend on fruit consumption for their nutritional supplements, while others may have alternative food resources besides fruits (Carnicer et al. 2009, Schleuning et al. 2011). These differing traits can influence the dynamics and stability of plant-frugivore interactions and thus the process of seed dispersal especially in the face of habitat fragmentation (Cramer et al. 2007, Spiegel & Nathan 2007).

Previous studies on the impacts of habitat fragmentation on ecological processes have focused more on measures of species diversity that only include information on the presence and abundance of species (e.g. Hector 1999, Gould & Walker 1999). However, a decrease or increase in species richness may not always mean there will be corresponding changes in functional diversity (Greenberg et al. 2000, Perfecto et al. 2004). Moreover, the influence of species richness on ecosystem function has been shown to largely depend on the traits and niches filled by species (Cadotte et al. 2011). In this case, the impact of habitat fragmentation and management practices on ecological processes is likely to be stronger if it changes the functional diversity rather than their species richness per se (Naeem et al. 2000, Cadotte et al. 2011). For example, while large dispersers have been shown to have the capacity to transport large proportions of seeds over long distances, their movements may be restricted by the magnitude of fragmentation (Peres 2000, Cramer et al. 2007). This may particularly disadvantage larger seeded plants that depend on larger dispersers for the transportation of their seeds (Moran et al. 2004, Cramer et al. 2007). Therefore, understanding the consequences of habitat fragmentation on the functional diversity of frugivores communities is paramount for the sustenance of seed dispersal processes (Cramer et al. 2007, Schleicher et al. 2011). In this context, it is also important to assess the impact of fruit or seed handling by various frugivorous species on germination

Effects of seed ingestion by frugivorous birds on germination success

The fruit handling behaviour of frugivorous birds plays a key role in determining their contribution to the seed dispersal process (Jordano & Schupp 2000). Frugivores that can swallow whole fruits, transport and defecate intact seeds in suitable habitats are often regarded as legitimate dispersers (Jordano & Schupp 2000). Whether or not fruit consumption by birds translates into successful seed dispersal is still a subject of much debate. Successful seed dispersal involves not only the removal of fruit from a source plant and depositing the seed into suitable sites, but also the ability of the deposited seeds to germinate and establish seedlings after passage through digestive tracts of birds (Herrera & Jordano 1981, Schupp 1993). Evidence from previous studies show either neutral (Howe & Vande Kerckhove 1981, Barnea et al 1992), positive (e.g. Clergeau 1992, Murray et al

1994) or negative (e.g. Valido & Nogalas 1994, Crossland & Vander Kloet 1996) effects of gut treatment on the germination patterns of seeds from various plant species. The reasons for these differing results are still not universally clear, but a few studies suggest that this could be explained by differences in functional traits of various plants (e.g. fruit morphology) and frugivorous species (Treveset 1998, Miller 1995, Jordano 2000). Therefore, taking these traits of plants and frugivorous into account when studying germination patterns of ingested seed can help to predict which frugivorous species contribute to the seed dispersal of which plant species. One way of doing this can be to feed fruits from different plant species to different species of frugivores (Schleicher et al. 2011). Understanding the abilities of different frugivore species within seed dispersal communities to contribute to plant recruitment will help to predict the impacts of fragmentation on forest regeneration, particular if habitat fragmentation affects the structure and functional diversity of seed dispersal communities to which these frugivores belong.

Aims of the thesis

In this thesis I investigated plant-frugivore interactions in a highly modified landscape in and around Vernon Crookes Nature Reserve (VCNR), located within KwaZulu Natal province, South African. This region comprises clusters of remnant natural scarp forest patches surrounded by dissimilar matrix habitats, notably, natural forest, natural grassland and commercial sugarcane monocultures. Therefore, it was a suitable area for undertaking this study, as it allowed for comparison of ecological processes between clusters of forest patches of different matrix habitats.

I compared (i) the structure of plant-frugivore interaction networks and (ii) functional diversity of frugivore communities within these networks. Moreover, I experimentally tested the impact of seed treatment in the digestive tracts of avian frugivorous to assess the importance of this specific trait (of seed treatment) on germination of dispersed seeds.

This thesis comprises comprise three major chapters (2 - 4) which can be read independently. Each chapter is structured like a journal publication containing an abstract, introduction, followed by the methods, results, discussion and a conclusion. The thesis closes with the general conclusions (chapter 5) derived from three major chapters (2 - 4).

The first major chapter (2) examines the consequences of forest patch quality and matrix habitat on the structure and stability of plant-frugivore networks in the fragmented forest landscapes VCNR. To do this, I identified all fleshy fruiting plant species across forest patches surrounded by variable matrix habitats and assessed their interaction frequencies with avian frugivore species. These data were arranged in quantitative interaction matrices to construct plantfrugivore interaction networks. Different network parameters were used to compare the network structures among forest patches.

The second major chapter (3) tests the effects of forest patch quality and matrix habitat on functional diversity of frugivore communities. Using the same data set as in chapter 2, I recorded the functional diversity of frugivore species and compiled these data in a species-trait matrix.

Then, I determined the effect of forest patch quality and matrix habitat on the species richness and functional diversity of these frugivorous communities.

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