Do Camelthorn Trees Use Sociable Weavers to Forage for Nutrients?

Kervin D. Prayag PRYKER001 Do camelthorn trees use sociable weavers to forage for nutrients?

BIO4000W (Hons) Department of Biological Sciences University of Cape Town

Supervised by: Michael D. Cramer (Department of Biological Sciences, UCT) Robert L. Thomson (Percy Fitzpatrick Institute of African Ornithology, UCT) November 2016 Plagiarism declaration

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Kervin Deveshwar Prayag

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Abstract “Islands of fertility” result from focussing of water and nutrients around many shrub- or tree- savanna species due to plant foraging for resources. Plant-animal feedbacks may amplify the development of such islands through environmental modification due to, for example, faunal deposition of nutrients and seeds. Fauna resident within vegetation clumps are likely to exert stronger feedbacks on their hosts than itinerant species. We studied the relationship between camelthorn trees (Vachellia erioloba) and the spectacular colonial nests of sociable weavers (Philetairus socius) in the Tswalu Kalahari reserve in the Northern Cape, South Africa. We hypothesized that nutrient inputs from the sociable weaver nests have a positive effect on tree growth and nutrient status. We also hypothesized that nests have negative consequences for the trees through reduced foliar canopies and increased branch fall. We measured tree leafiness, foliar and nutrient contents and δ15N values across pairs of trees with and without nests. We also measured sub-canopy vegetation cover in the islands of fertility below the trees. There were no significant differences in foliar N, P and K between nest and control trees, although δ15N differed strongly. Trees with nests, however, had 27% higher leafiness of terminal branches. Trees thus utilise the nutrients made available through bird faeces for growth, although they do not accumulate more foliar nutrient. Canopy volume was, however, reduced in trees with nests due to these occupying large volumes and to branch fall. Sub-canopy vegetation cover was surprisingly decreased. We conclude that the benefits to the camelthorn trees through faunal deposition of nutrients does not come without costs to the trees, and that this plant-animal interaction has measurable effects on the associated sub-canopy vegetation.

Keywords: sociable weaver, camelthorn, semi-arid savanna, plant-animal interactions, positive feedbacks, faunal nutrient input

TABLE OF CONTENTS

Plagiarism declaration i

Abstract ii

Introduction 1

Materials and methods 4

Study system 4

Sampling procedure 4 Loss of biomass 4 Foliar canopies 5 Sub-canopy vegetation 5 Biomass accumulation, foliar nutrient concentrations and foliar N ratios 5 Biological nitrogen fixation 6

Data analyses 7

Results 8

Discussion 9

Acknowledgements 13

References 14

List of figure captions 19

Figures and tables 21

Appendix 31

Introduction In arid and semi-arid environments where resources are scarce, conditions can be limiting in terms of growth and reproduction for plants. In these environments, plants are known to use diverse strategies to gather resources. Such strategies include deep roots, biological nitrogen fixation, and inverse hydraulic lift (Schulze et al. 1991; Jackson et al. 1996; Schulze et al. 1998; McCulley et al. 2004). The use of these strategies have been documented for camelthorn trees (Vachellia erioloba) in arid and semi-arid regions (Schulze et al. 1991; Canadell et al. 1996; Seymour 2008). Camelthorns are an iconic and dominant tree species in arid and semi-arid regions of Southern Africa, and are critical to animal and plant communities in the area (Coates Palgrave 2005). In its Kalahari range, camelthorns are known to host large nest colonies of the gregarious bird species Philetairus socius, commonly called sociable weavers. In arid and semi-arid savannas, in addition to its other resource acquisition strategies, the camelthorn tree may be able to forage for nutrients from the soils enriched by the deposition of faeces below its canopy when hosting a sociable weaver colony.

Interactions between plants and animals are abundant in natural systems with important impacts on structure, function and diversity of ecosystems through processes such as pollination, seed dispersal, habitat provisioning or nutrient cycling (Ehrlich and Raven 1964; Quek et al. 2004; Tiffney 2004; Bascompte and Jordano 2007). Interactions can range from being mutually beneficial for both partners, to being one-sided and benefit only the one partner (Andersen and Braithwaite 1996). For example, plant-pollinator interactions are often mutually beneficial: in return for pollinating the flowers, the pollinator is rewarded with nectar (Ramírez et al. 2011). Positive interactions can involve cost and benefits for either one, or both of the partners (Addicott 1986). As an example, grazing pressure by ruminants leads to a loss of biomass in plants, but deposition of faeces by the animals (faunal nutrient input) can increase the nutrients available to the plants (Whitehead 2000). The plants can therefore outweigh the costs of grazing pressure by investing in this increase in resource availability to increase productivity, nutrient content and reproductive output (van der Wal et al. 2004). Other potentially mutualistic plant-animal interactions are the ones between birds and plants. For example, a tree hosting an insectivorous bird species can experience decreased pressure from insect herbivory (Mäntylä et al. 2011). Costs and benefits to camelthorn trees hosting sociable weavers have however not yet been documented.

In the interaction between sociable weavers and camelthorns, the benefit to the birds through habitat provisioning by camelthorns has previously been documented: as one of the few very large tree species in arid and semi-arid savannas, the camelthorn is one of the limited structures on which sociable weavers can build their colonies (Dean et al. 1999; Spottiswoode 2009). Sociable weaver colonies can be very large in size and one nest can host up to 500 individuals (Maclean 1973; Covas et al. 2004). Faeces and nest material continuously falling from the large nest colonies therefore result in very high levels of localized faunal nutrient input enrich soils in nutrients beneath the camelthorn trees (Dean et al. 1999). Studies have shown that in addition to enriching soils in nutrients in terrestrial systems, seabird guano can also alter the soil nitrogen isotopic ratio (δ15N) (Wainright et al. 1998; Szpak et al. 2012). Using the 15N natural abundance technique, it was shown that plants make use of nutrients from these soils enriched by guano deposition (Wainright et al. 1998). In a tandem study investigating the soil chemistry below camelthorns trees with nests and without nests, it was found that soil nutrients and 15N abundance increased in the presence of a nest (du Toit 2016). It remains unknown whether the δ15N in camelthorns is similarly altered when the tree hosts a sociable weaver nest, or whether the tree makes use of the abundant nutrients for growth.

In Kalahari ecosystems, camelthorn trees are known as ecosystem engineers as they create islands of fertility below their canopies which provides favourable conditions for sub-canopy plant species to establish and grow (Dean et al. 1999; Seymour 2006). Faunal nutrient input through the deposition of sociable weaver faeces below the tree canopies can lead to an enhancement of these islands of fertility. There is also increasing evidence that sociable weaver colonies can benefit other animal species through food and habitat provisioning (Rymer et al. 2014). Examining the costs and benefits to camelthorns when hosting sociable weaver nest colonies is therefore of importance, as camelthorns, and potentially sociable weavers, play an important role in these Kalahari ecosystems.

In the present study, we examine the costs and benefits to camelthorns of hosting sociable weaver nests. We also examine potential effects of this plant-animal interaction on the sub-canopy vegetation in the islands of fertility below the trees. We hypothesize that nutrient inputs through the deposition of sociable weaver faeces have a positive effect on tree growth and foliar nutrient status, and an effect on foliar δ15N. We also hypothesize that nests have negative consequences

2 for the trees through reduced foliar canopies and increased branch fall. Lastly, we hypothesize that nutrient inputs from the sociable weaver nests will increase sub-canopy vegetation cover below the trees. To test these hypotheses, camelthorn tree growth, foliar nutrient concentrations, foliar nitrogen isotopic ratios, change in biomass and sub-canopy vegetation cover of camelthorn trees with and without nests were measured, analyzed, and compared.

Materials and methods Study system The study was undertaken in the semi-arid Tswalu Kalahari reserve in the Northern Cape, South Africa (27°13′30″S and 22°28′40″E, altitude 1020–1586masl) (Figure 1). This savanna system is characterized by reddish-brown sandy soils with an open canopy of trees and shrubs that includes species such as Vachellia erioloba, Vachellia mellifera and Boscia albitrunca, and with a sparse grassy layer including species such as Schmidtia papophoroides, Stipagrostis uniplumis and Aristida congesta. Mean annual precipitation is ca. 289 mm with a mean annual temperature of 17.1°C. The reserve is home to an extensive range of fauna including large mammals such as giraffe (Giraffa camelopardalis), wildebeest (Connochaetes taurinus), gemsbok (Oryx gazella) and springbok (Antidorcas marsupialis), and smaller mammals such as yellow-tailed mongooses (Cynictis penicillata), ground squirrels (Xerus inauris) and meerkats (Suricata suricatta). Camelthorn trees with sociable weaver nests are an iconic feature of this landscape. Ungulates such as gemsbok (O. gazella) and wildebeest (C. taurinus) resting in the shade under the canopies of these trees is a recurrent sight in the reserve (K. Prayag, pers. obs.).

Sampling procedure Within the reserve, a total of 18 camelthorn trees with nests were selected for the purpose of this study. Each of these trees with nests were paired (n = 36) with camelthorn trees without nests, but which were similar in height, diameter at breast height (which served as a proxy for age of the tree), and which were no more than 200 m in distance from the nest tree. In each pair, the branch on which the nest was built was identified and paired with a similar-sized and oriented branch in the tree without a nest (hereafter referred to as the ‘nest branch’). Cross-sectional areas of the main tree trunk and of the nest branches were calculated by using diameter at breast height and the diameters at base of nest branches respectively. The height of all 36 trees were measured using a hypsometer (Nikon Forestry Pro, NIKON VISION CO., LTD, Tokyo Japan). The GPS coordinates of the trees were recorded.

Loss of biomass At each tree, the number and diameter at the base of fallen branches, if present, were recorded. From these diameters, the summed cross-sectional areas of all fallen branches were calculated.

The summed cross-sectional areas of fallen branches were standardized by the respective cross- sectional areas of the main trunk of the trees (‘branch fall’) from which they had fallen.

Foliar canopies Photographs of the nest branches were taken at a height allowing lateral views of these branches using a digital camera. A 1-meter scale was included in the frame of each of these photographs. A grid with 10x10 cm cells (using the 1-meter scale as reference) was then overlaid onto the photographs using Adobe Photoshop CS5 Extended (Adobe Systems Incorporated, Version 12.0). Using a color-coding system, each cell was filled according to their content (either nest or leaf) on the photographs. The respective color-coded cells were then counted using the ‘Magic Wand’ and ‘Count’ tools of Adobe Photoshop CS5 Extended. From these counts, nest and foliar two- dimensional areas on nest branches were obtained. These two-dimensional areas were standardized by the cross-sectional areas at base of the respective nest branches.

Sub-canopy vegetation Photographs of the sub-canopy vegetation below each tree were taken. In each of these photographs, the percentage of sub-canopy vegetation cover was then visually estimated. Below camelthorn trees with nests, we observed the presence of circular barren patches in the sub-canopy vegetation directly beneath the sociable weaver nests. These patches were not quantified.

Biomass accumulation, foliar nutrient concentrations and foliar N ratios On each tree, four terminal branches, each facing one of the four cardinal directions, were identified and collected. The terminal branches were stripped of their leaves, and the subtending branch diameter measured. The fresh weights of these leaves were expressed as a function of the diameters at base of the respective terminal branches from which they were stripped. The leaves were dried in a domestic oven at 70°C for 36 hours and their dry weights were recorded. These leaves were stored and later used for nutrient and isotopic analyses (see below).

Leaf samples were taken from each of the 18 B. albitrunca trees located almost equidistant between the camelthorn trees in a pair. These leaf samples were then dried in a domestic oven at

70°C for 36 hours, stored, and later used as a non-N2-fixing species reference in the nitrogen isotopic analyses (see below).

The dried leaf samples from both the camelthorn and B. albitrunca trees were crushed to a powder using a ball-mill (MM200 Retsch®, Haan, Germany). The leaf powder samples were placed in Perspex rings sealed with 4 μm Polypropylene thin film (Chemplex Industries Inc, Florida, USA) and introduced to a SPECTRO XEPOS XRF spectrometer (SPECTRO, AMATEK materials analysis division, Kleve, Germany). Analyses were conducted using the X-LabPro 5 software, which incorporates the universal ‘Turbo Quant Powders’ method. The instrument was calibrated by using a certified standard GBW07312 (National Research Center for CRMs, Beijing, China), for which elemental concentrations were obtained from NOAA Technical memorandum NOS ORCA 68 (1992). Only the elements that were within the machine’s detection limits were included. These elements were K, P, Ca, Mg, Zn and Fe.

Foliar δ15N and N concentration for camelthorn trees with nests, camelthorns trees without nests and B. albitrunca trees were determined using mass spectrometry. Approximately 2mg of a leaf powder sample was weighed into a tin capsule (5x9mm Säntis Analytical, Teufen, Switzerland). The samples were then combusted in a Flash 2000 organic elemental analyser and the gases passed to a Delta V Plus isotope ratio mass spectrometer (IRMS) via a Conflo IV gas control unit (all from Thermo Scientific, Bremen, Germany). Three in-house standards and one IAEA (International Atomic Energy Agency) standard (USGS25) were used to calibrate the results. Nitrogen was expressed relative to atmospheric nitrogen.

Biological nitrogen fixation 15 Using the average foliar B. albitrunca δ N value as a non-N2-fixing species reference, the biological N2-fixation of all the camelthorn trees were calculated. The calculations were done using the following formula:

δ15N퐵 − δ15N퐶 퐵푁퐹퐶 = ( ) ∗ 100 δ15N퐵 − 퐵푣푎푙푢푒 where:

- 퐵푁퐹퐶 is the N2-fixation of a nest tree or a tree without a nest

15 - δ15N퐵 is the average foliar δ N of B. albitrunca trees in this study

15 - δ15N퐶 is the foliar δ N of a nest tree or a tree without a nest, and

- 퐵푣푎푙푢푒 is the isotopic fractionation of the N2-fixation process.

Top soil layer δ15N values below five pairs of camelthorn trees (these tree-pairs were part of our sample) were obtained from soil analyses done by du Toit (2016). Using these top soil layer δ15N values as a proxy, the N contribution of sociable weaver faeces to the five nest trees in the five tree-pairs was estimated. These estimations were done using the following formula:

δ15N − δ15N 푇표푝 푠표푖푙 푙푎푦푒푟 푁 푐표푛푡푟푖푏푢푡푖표푛 = ( 퐶퐶 퐶푁) ∗ 100 δ15N푆퐶 − δ15N푆푁 where:

- 푇표푝 푠표푖푙 푁 푐표푛푡푟푖푏푢푡푖표푛 is the top soil layer N contribution to a nest tree

15 - δ15N퐶퐶 is the foliar δ N value of a tree without a nest

15 - δ15N퐶푁 is the foliar δ N value of a nest tree

15 - δ15N푆퐶 is the soil δ N value below a tree without a nest, and

15 - δ15N푆푁 is the soil δ N value below a nest tree.

Data analyses All statistical analyses were performed using R statistical software (R Core Team 2016). Tree height and diameter at breast height (DBH) were compared using paired t-tests to determine whether the pairs were similar enough for fair comparisons to be made. A non-significant difference in height and DBH indicated fair comparisons.

Paired t-tests were used again to test whether any significant differences existed in six paired measured variables (height of tree, DBH, foliar dry weight, two-dimensional foliar area, branch fall, and percentage sub-canopy vegetation cover) between camelthorn trees with and without nests. Significant differences in these variables indicated direct or indirect effects of the presence sociable weaver colonies.

A one-way Analysis of Variance (ANOVA) followed by a post-hoc Tukey test was done in order to determine whether there were any significant differences in foliar δ15N between camelthorn trees with nests, camelthorn trees without nests, and B. albitrunca trees. The post-hoc Tukey test was done using the ‘agricolae’ package in R (Mendiburu 2016). Significant differences indicated direct or indirect effects of the presence sociable weaver colonies on foliar δ15N of these trees.

Results Tree height and stem circumference did not differ significantly (p > 0.05) between camelthorns with nests and camelthorns without nests (Table 1). Foliar dry weight expressed as a function of the diameter at base of respective terminal branch were found to be significantly greater (p < 0.05) on camelthorns with nests (Table 1; Figure 2). The two-dimensional foliar areas expressed as a function of cross-sectional area at base of nest branches were found to be significantly lower (p < 0.05) in camelthorns with nests (Table 1; Figure 3). Two-dimensional areas for two tree-pairs could not be obtained as it was not possible to distinguish the nest branches from other branches on the photographs of the nest branches of these trees. Summed cross-sectional area of fallen branches was significantly higher (p < 0.05) in camelthorns with nests (Table 1; Figure 4). Sub- canopy vegetation cover in the islands of fertility below the camelthorns was found to be significantly lower (p < 0.05) under trees with nests (Table 1; Figure 5).

There were no significant differences (p > 0.05) in foliar concentrations of N, P, K, Mg, Fe, Ca and Zn between camelthorn with nests and camelthorns without nests (Appendix 1). Foliar δ15N of B. albitrunca trees was significantly higher (p < 0.05) than foliar δ15N of camelthorns without nests (Figure 6). Foliar δ15N of camelthorns with nests was significantly higher (p < 0.05) than foliar δ15N of camelthorns without nests (Figure 5). No significant difference (p > 0.05) was observed between foliar δ15N of B. albitrunca trees and camelthorns with nests (Figure 5). A strong 2 negative correlation (R = 0.95) was observed between biological N2 fixation of camelthorns with nests (n = 5) and estimated faeces N contribution to the trees (Figure 7). As faeces N contribution increases, N2-fixation decreases.

Discussion Animals concentrating nutrients such as N, P and K in soils through the deposition of faeces or dung can induce responses in plant growth (Bazely and Jefferies 1985; van der Wal et al. 2004). Productivity in plants has been found to increase in soils enriched in N, P and K through faunal nutrient input (Anderson and Polis 1999; Sheldrick et al. 2003). Similarly, the deposition of faeces by sociable weavers led to an increase in vegetative growth in camelthorn trees hosting a nest. However, the large sizes of the nests led to the replacement of foliar canopy, as well as increased branch fall. The benefits of hosting a sociable weaver colony therefore do not come without costs for the camelthorn trees. The decrease in sub-canopy cover due to the presence of a nest shows that the association between camelthorns and sociable weavers can have impacts on the ecosystem structure in the Kalahari ecosystems.

In the reserve, it was found that soil concentrations of N, P and K were significantly higher below trees with nests, compared to trees without nests (du Toit 2016). The observed increase in foliar dry weight expressed as a function of subtending branch diameter at base observed in the nest trees strongly suggests that faunal nutrient input from the sociable weavers have direct positive effects on the camelthorn trees. Furthermore, foliar nutrient status in camelthorn trees did not differ between those with nests and those without, suggesting efficient allocation of nutrients to vegetative growth, rather than luxurious consumption thereof (Millard 1988; Lawrence 2001; Tripler et al. 2002). The increase in vegetative growth observed in nest trees therefore supports the hypothesis that in return for habitat provisioning to the sociable weavers (Dean et al. 1999; Spottiswoode 2009), the camelthorn trees can benefit from the input of nutrients through deposition of faeces below their canopies.

Ammonia volatilization of seabird guano has been found to enrich soils in terrestrial ecosystems with 15N (Mizutani et al. 1986; Mizutani and Wada 1988). We postulate that continuously falling faeces from sociable weaver nests can have a similar enriching effect on the soils directly below the trees in which they are nesting. Data from a study by du Toit (2016) suggest that soils below camelthorn nest trees are more enriched with 15N compared to soils below camelthorn trees without nests. Using the 15N abundance technique, it is possible to trace the source of nitrogen uptake of plants (Wainright et al. 1998). Terrestrial plants exposed to soils enriched with 15N by seabird guano experienced an increase in δ15N (Wainright et al. 1998; Szpak et al. 2012),

9 suggesting uptake of nutrients by the plants from these 15N-enriched soils. Similarly, we found that leaves of camelthorn trees hosting sociable weaver nests had higher δ15N compared to camelthorn trees without nests, supporting the hypothesis that nutrient inputs from the sociable weavers increases foliar δ15N in trees with nests. The increase in foliar δ15N adds to the evidence supporting the benefit to the trees through the uptake of nutrients from the soils enriched by the bird faeces.

Since camelthorn trees are nitrogen fixers, these differing nitrogen isotopic ratios could also be as a result of decreasing biological N2 fixation. Leguminous plant species fixing N2 have been reported to have lower δ15N than non-leguminous plant species (Schulze et al. 1991). Along an aridity gradient in Namibia, it was found that camelthorn trees had lower δ15N than B. albitrunca (non-legume) trees (Schulze et al. 1991). We observed a similar pattern at our study site between camelthorns without nests and B. albitrunca trees. In addition, we found a negative correlation 15 between N2-fixation and estimated faeces N contribution to the trees with nests. Higher foliar δ N in nest trees compared to trees without nests could therefore also be the consequence of decreased

N2-fixation as a result of preferential uptake of N from the nutrient-enriched soils. The calculation of N2-fixation can however be problematic (Spriggs et al. 2003), particularly regarding the choice of a suitable non-N2-fixing reference species. The most suitable reference species would be one with as many physiological properties as possible kept consistent between the reference species and the leguminous species. Failure to acquire a suitable non-N2-fixing reference species may lead to imprecise N2-fixation estimates (Shearer and Kohl 1986; Bremer et al. 1993). Sociable weavers also construct their nests in B. albitrunca trees, and these have been observed in the reserve (K. Prayag, pers. obs.). The use of foliar δ15N of the B. albitrunca trees with nests as a reference would have led to more accurate estimations of N2-fixation for nest trees. Nonetheless, the rough estimations of N2-fixation and its strong negative correlation with faeces N contribution also adds to the evidence in support of potential benefits to the trees.

Trees with nests experienced more numerous branch fall events expressed as a function of cross- sectional area of the main tree trunk. Hosting a nest can therefore lead to loss of biomass. Sociable weaver nests can become very large in size and extend onto multiple branches in camelthorn trees (Spottiswoode 2009). These large nests often result in the branches on which they are constructed

10 to buckle, and eventually break (Figure 8), purely as a result of weight. In the reserve, cases of host trees toppling over as a consequence of hosting large sociable weaver nests have also been reported (R. Thomson, pers. comm.). To the best of our knowledge, this type of mechanical damage caused by birds to their host tree has not previously been reported or investigated in the literature. A decrease in foliage area expressed as a function of nest branch cross-sectional area is also observed in trees with nests. In some instances, large sociable weaver nests were found to completely replace the foliage of the branch on which they were built (Figure 9). Sociable weavers tend to choose large camelthorn trees to build their nests (Dean et al. 1999). The loss of entire canopy sections can have serious consequences for these trees, such as a reduction in photosynthetic capacity (Bolstad et al. 2001). In the plant-animal interaction between sociable weavers and camelthorns, the observed damage to the trees caused by the birds bears certain similarities to the damage inflicted on marula trees (Sclerocarya birrea) by African elephants (Loxodonta africana). Elephants aid the dispersal and germination of marula seeds after consuming them (Midgley et al. 2012), but as a consequence, marula trees often sustain branch and bark damage through these encounters (Gadd 2002). The observed increase in branch fall and decrease in foliar canopy in camelthorn nest trees supports the hypothesis that benefits of hosting a sociable weaver colony are accompanied by certain costs for the camelthorn tree.

Surprisingly, under trees with nests, sub-canopy vegetation cover in the islands of fertility was found to decrease. Previous studies have documented the manuring effects of seabird guano (Smith 1978; Ellis 2005). The study by du Toit (2016) has shown an increase in soil concentrations of N, P and K under trees with nests. This could potentially enhance the islands of fertility created by the trees. Furthermore, in the reserve, it has been reported that the number of visits to camelthorn trees by ungulates increases when the trees host a nest (A. Lowney, pers. obs.), possibly to rest under the shade provided by the nests during the heat of the day. These visits may also contribute to increased nutrient inputs into the islands of fertility through deposition of herbivore dung (Wal et al. 2004; Bazely and Jerries 1985). However, these trends do not correspond with the observations made of sub-canopy vegetation cover beneath camelthorn trees hosting nests. Data from the study done by du Toit (2016) suggests that soils directly below the nests had lower water infiltration rates than surrounding soils. These lower infiltration rates are suggested to be as a result of the continuously falling faeces and nest material forming a

11 hydrophobic layer on these soils (du Toit 2016). Low infiltration rates can impede on the ability of sub-canopy plant species to establish and could result in overall decreased sub-canopy cover under trees with nests. The hypothesis that nutrient inputs through the deposition of sociable weaver faeces increase sub-canopy vegetation cover in the islands of fertility associated with the camelthorn trees is therefore not supported. In arid and semi-arid environments with open layers of trees or shrubs, such as at our study site, soil properties such as moisture and nutrient availability are heterogeneously distributed (Schlesinger et al. 1990), usually as a result of biotic concentrating mechanisms (Stock et al. 1999). The concentration of nutrients at the trees by the fauna can potentially lead to a reinforcement of this heterogeneity, thus impacting on the ecosystem structure in the reserve. The inverse correlation between presence of a nest and sub-canopy vegetation cover as well as the potential reinforcement in heterogeneous resource distribution provides some insight into how the interaction between camelthorns and sociable weavers can influence ecosystem structure in arid and semi-arid savannas.

Conclusion

The present study is, to the best of our knowledge, the first to provide evidence for costs and benefits to camelthorn trees associated with hosting sociable weaver nests colonies. In this plant- animal interaction, nutrient inputs through faunal deposition of dung or faeces can largely facilitate the process of resource gathering for the camelthorns, especially in arid and semi-arid environments. However, this does not come without costs for the trees, as demonstrated by increased branch fall and reduction of canopy foliage. This study has also shown measurable negative effects of sociable weaver colonies on sub-canopy vegetation cover in the islands of fertility below the camelthorn trees. Positive interactions, such as the facilitation of sub-canopy plant species by camelthorns, are predicted to become more important under conditions of increased environmental and climatic stress (Crain and Bertness 2006). In light of changing climatic conditions, understanding the effects of hosting a sociable weaver nest on both the camelthorn tree and its associated sub-canopy vegetation is therefore of importance for the conservation of diversity in these areas.

Acknowledgements I would like to express my gratitude to the Oppenheimer family and Tswalu Kalahari Reserve for allowing us to conduct our research on their property – there were more exciting animal encounters than was expected, which made field work even more memorable and enjoyable. My sincere thanks to Anthony Lowney for his company, for taking care of us during our stay at Tswalu Kalahari, and for his assistance and ‘expertise’ in the field. Thanks to my classmate and field work partner, Carla du Toit, for her insight into the soils analysis. Thanks also to Ian Newton for his assistance with the nitrogen isotope analyses. I would like to thank Simon Power, for his extremely valuable input and for being a researcher whose standards I aspire to; Kirsten Packer, for the brainstorming sessions, and her assistance with graphing in R; Jacques Nel and Zander Venter, for their valuable inputs; and Hana Petersen for her skill in generating simplistic maps, for her moral support, and her willingness to proofread. And finally, my utmost respect and gratitude goes to my supervisors, Mike Cramer and Rob Thomson – great company, while also inspiring me to broaden my thinking and constantly improve myself and my research.

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List of figure captions Figure 1: Map showing the location of the study site with biomes of South Africa (Mucina and Rutherford 2006).

Figure 2: Foliar dry weight expressed as a function of the diameters at base of the respective terminal branches for Vachellia erioloba with and without nests. The boxes and horizontal lines represent the first and the third quartiles and the medians, respectively. The whisker represents 1.5 x the interquartile range and outliers above/below are shown as open circles. The means (diamond) are also shown. Different letters indicate significant differences determined by a paired t-test.

Figure 3: Two-dimensional foliar areas expressed as a function of the cross-sectional areas of the respective ‘nest branches’ for Vachellia erioloba with and without nests. The boxes and horizontal lines represent the first and the third quartiles and the medians, respectively. The whisker represents 1.5 x the interquartile range and outliers above/below are shown as open circles. The means (diamond) are also shown. Different letters indicate a significant difference determined by a paired t-test.

Figure 4: Cross-sectional area of fallen branches expressed as a function of cross-sectional areas at breast height of respective trees for Vachellia erioloba with and without nests. The boxes and horizontal lines represent the first and the third quartiles and the medians, respectively. The whisker represents 1.5 x the interquartile range and outliers above/below are shown as open circles. The means (diamond) are also shown. Different letters indicate a significant difference determined by a paired t-test.

Figure 5: Sub-canopy vegetation cover (%) in the islands of fertility under Vachellia erioloba with and without nests. The boxes and horizontal lines represent the first and the third quartiles and the medians, respectively. The whisker represents 1.5 x the interquartile range and outliers

19 above/below are shown as open circles. The means (diamond) are also shown. Different letters indicate a significant difference determined by a paired t-test.

Figure 6: The variation in foliar δ15N between Vachellia erioloba with and without nests, and Boscia albitrunca trees. The boxes and horizontal lines represent the first and the third quartiles and the medians, respectively. The whisker represents 1.5 x the interquartile range and outliers above/below are shown as open circles. The means (diamond) are also shown. Different letters indicate significant differences determined by one-way ANOVA followed by post-hoc Tukey tests.

Figure 7: Biological nitrogen fixation (%) relative to Boscia albitrunca for Vachellia erioloba trees with nests (n = 5), with respect to top soil layer N contribution (%). The grey band represents the 95% confidence limit.

Figure 8: Photograph showing branch fallen (left) from a Vachellia erioloba tree due to the presence of a Philetairus socius nest at Tswalu Kalahari in Northern Cape, South Africa.

Figure 9: Photograph illustrating the complete replacement of foliar canopy by a Philetairus socius nest on the branch of a Vachellia erioloba tree at Tswalu Kalahari in Northern Cape, South Africa.

Figures and tables Table 1: Summary statistics of the paired t-tests done to check for significant differences in the paired data between Vachellia erioloba with and without nests. Asterisks indicate statistical significance (p < 0.05).

Test Mean (± SD) Mean (± SD) Degrees of p-value with nest without nest freedom

Height (m) 5.52 (± 0.97) 5.30 (± 0.66) 17 0.282

DBH (m) 0.51 (± 0.16) 0.58 (± 0.20) 17 0.208

Foliar dry weights 0.54 (± 0.22) 0.43 (± 0.19) 17 0.009* (kg.m-1)

Two-dimensional 52.65 (± 37.46) 76.88 (31.58) 15 0.0181* foliar areas

Branch fall 0.32 (± 0.51) 0.01 (± 0.04) 17 0.016*

Sub-canopy vegetation cover 39.83 (± 26.17) 60.58 (19.98) 17 0.003* (%)

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Appendix Appendix 1: Summary statistics of the paired t-tests done to check for significant differences in foliar concentrations of N, P, K, Ca, Mg, Zn and Fe between Vachellia erioloba with and without nests.

Mean with nest Mean without Degrees of Element p-value (± SD) nest (± SD) freedom N 2.662 (± 0.185) 2.716 (± 0.185) 17 0.318

P 0.144 (± 0.022) 0.148 (± 0.028) 17 0.646

K 1.332 (± 0.419) 1.339 (± 0.458) 17 0.952

Ca 2.923 (± 0.811) 3.223 (± 0.851) 17 0.081

Mg 0.418 (± 0.208) 0.357 (± 0.189) 17 0.179

Zn 0.003 (± 0.001) 0.003 (± 0.001) 17 0.247

Fe 0.036 (± 0.023) 0.030 (± 0.008) 17 0.247