Seed dispersal potential of jackals and foxes in semi-arid habitats of South Africa
Introduction
Seed dispersal is an important aspect of the ecology of plant communities. To aid dispersal, some plant species have evolved fleshy fruits around seeds (hereafter fruit plants), which are consumed for a nutritional reward by a wide variety of animals (Krefting and Roe, 1949; Herrera, 1984; Howe, 1986; Willson, 1993). Through defecation, animals deposit the seeds at various distances from the source plant, called seed shadows, which are dependent on animal movements and gut retention times (Koike et al., 2010). Successful germination and seedling establishment within seed shadows is greatly affected by the microhabitat of the animal's defecation sites (Chavez-Ramirez and Slack, 1993), and sometimes secondary movements of seeds after defecation (Koike et al., 2012). By influencing the spatial distribution and demography of the plants they feed on, seed dispersers may shape the vegetative landscape and contribute to the natural regeneration of ecosystems (Wisz et al., 2013; Baños-Villalba et al., 2017). Most research on fruit dispersals has focused on birds, which are often considered the most important seed dispersers in tropical regions (Baños-Villalba et al., 2017; Corlett, 2017; Sebastián-González, 2017). However, in temperate and semi-arid regions, mammalian species were found to disperse seeds of fruit plants farther than birds, and at greater quantities (Jordano et al., 2007). In fact, some fruit plants may have evolved to have their seeds consumed exclusively by mammals instead of birds (Zhou et al., 2013). Among mammals, several species of omnivorous Carnivora have been shown to be major dispersers of seeds, including small and medium-sized Canidae (Willson, 1993). For example, coyotes (Canis latrans) were found to be the most highly frugivorous north temperate mammal, and this species is likely to be among the quantitatively most important mammalian dispersers of fruit plants in North America (Willson, 1993). Similarly, red foxes (Vulpes vulpes) and corsac foxes (V. corsac) were found to be important dispersers of fruit plants in semi-arid parts of southern Europe (Juan et al., 2006; Rosalino and Santos-Reis, 2009; Cancio et al., 2016) and central Asia (Murdoch et al., 2009), respectively.
In semi-arid regions of South Africa, there are three species of small and medium-sized canids that potentially could be major dispersers of fruit plants: cape foxes (Vulpes chama), bat-eared foxes (Otocyon megalotis), and black-backed jackals (Canis mesomelas). Although previous studies have confirmed that all three of these canid species regularly consume fruit (Kok, 1996; Klare et al., 2010, 2011; 2014; Kamler et al., 2012), their potential as important seed dispersers has received little attention. For example, bat-eared foxes, but not cape foxes and jackals, were reported to be a disperser of several species of fruit plants in semi-arid regions of South Africa (Milton and Dean, 2001). Only a few studies commented on the potential of black-backed jackals to assist with seed dispersal of fruit plants (Castley et al., 2001; Kaunda and Skinner, 2003). Clearly, more research is needed on the potential of canids to act as seed dispersers in semi-arid environments in South Africa, given the propensity of canids to act as major seed dispersers in other semi-arid regions of the world. Such information might especially be relevant for South Africa, where large carnivores have been extirpated over most of the country, leaving jackals, which can attain high densities, as the dominant predator in most ecosystems (Klare et al., 2010; Minnie et al., 2016).
The seed dispersal potential of canids in South Africa is relevant not only for the ecology of native fruit plants, but also for the ecology of alien mesquite (hybrids of Prosopis glandulosa and several other alien Prosopis spp.) which has invaded large areas of South Africa and is causing ecosystem-level changes in savannas (Dean et al., 2002; Milton et al., 2007; Shackleton et al., 2015; Van den Berg, 2010). In North America, coyotes were sometimes found to consume large amounts of honey mesquite (P. glandulosa) seeds in semi-arid areas, and they acted as a major disperser of this species within its native range (Meinzer et al., 1975; McClure et al., 1995). In South America, the diet of the Sechuran fox (Lycalopex sechurae) in desert habitat was dominated by P. juliflora seeds in some seasons (Asa and Wallace, 1990), and it was found to be a relevant seed disperser of this species (Escribano-Avila, 2019). Thus, jackals or foxes might be helping to facilitate the dispersal and expansion of Prosopis spp. within its non-native range in South Africa, although the consumption of Prosopis seeds by canids in South Africa has never been reported.
The defecation sites of animals within their seed shadows can greatly affect successful germination and seedling establishment (Reid, 1989; Chavez-Ramirez and Slack, 1993). For example, it was concluded that red foxes and grey foxes (Urocyon cinereoargenteus) in Texas, USA, had deposited scats in poor germination sites because >95% of the scats were found in open areas near or on dirt roads and trails where wildlife and livestock would trample them (Chavez-Ramirez and Slack, 1993). In contrast, scats deposited under the canopy of trees by other carnivores were considered favorable germination sites (Chavez-Ramirez and Slack, 1993). Similarly, coyotes in Oregon, USA, were found to defecate pinyon (Juniperus occidentalis) seeds in open areas, which are poor germination sites because pinyon seeds germinate best beneath shrubs (Schupp et al., 1997). Therefore, it is important to record information on the defecation sites when investigating the potential of canids to act as seed dispersers of fruit plants.
We describe the seasonal consumption of several species of fruit plants by cape foxes, bat-eared foxes, and black-backed jackals in South Africa. We also recorded information about their defecation sites to assess their potential as germination sites. This research was part of a larger study investigating the ecology of foxes and jackals; thus, the densities and home range sizes of the canid species on our study sites were known (Kamler et al., 2013b, 2017, 2019; Kamler and Macdonald, 2014). To estimate the seed dispersal potential of each canid species, we incorporated results about their fruit consumption and defecation sites, with information about their home range sizes and densities. This is the first detailed study of the seed dispersal potential of South African canids, and our results have relevance not only for the regeneration of native fruit plants in semi-arid regions, but also for the expansion of alien invasive Prosopis spp. as well.
Section snippets
Study species
This research was part of a larger study investigating the ecology and interspecific relationships of cape foxes, bat-eared foxes, and black-backed jackals on several study sites in South Africa (Kamler et al., 2012, 2013b; Klare et al., 2010, 2011, 2014). Capture, radio-telemetry monitoring, and scat collection were the primary methods used to investigate the ecology of each species. Results of the ecological findings allowed us to make post hoc investigations of their potential as seed
Results
On Benfontein, we collected 133 cape fox scats, 177 bat-eared fox scats, and 312 jackal scats. All canid species consumed fruit of Diospyros lycioides (bluebush) in every season, although frequency of consumption peaked in different seasons for each canid species: summer for bat-eared foxes, autumn for jackals, and winter for cape foxes (Table 2, Fig. 1). Overall, bat-eared foxes consumed D. lycioides fruit most frequently (14–42% of scats across seasons), followed by cape foxes (5–18%) and
Discussion
Both fox species and jackals consumed Diospyros lycioides berries on Benfontein throughout the year, indicating all three canid species are potential dispersers of this fruit. Previous research also showed that all three canid species frequently consumed D. lycioides berries (Kok, 1996). Reasons for the different seasonal peaks in consumption among canids on Benfontein were unclear, but may have been related to periods of fruiting and availability of main prey. Previous research on canids
Conclusions
In semi-arid savanna and shrubland of South Africa, seed dispersal of fruit plants by foxes and jackals is probably more significant than previously thought, especially given that bat-eared foxes and jackals each consumed and dispersed about 50 kg of fruit/km2. Compared to other mammalian species in semi-arid habitats, canids, especially jackals, attain relatively high densities, consume relatively large amounts of fruits, and have relatively large home ranges and movements, all of which
CRediT authorship contribution statement
Jan F. Kamler: Conceptualization, Writing - original draft. Unn Klare: Investigation, Writing - review & editing. David W. Macdonald: Writing - review & editing, Funding acquisition.
Acknowledgments
We thank De Beers Consolidated Mines for allowing us access to their properties, and providing support for this project. We also thank U. Stenkewitz for help with collecting scats, B. Wilson and McGregor Museum for providing logistical support, and an anonymous reviewer for helpful comments that improved the manuscript. Funding for JFK was provided by a Research Fellowship from the Wildlife Conservation Society, New York, and a Marie Curie Fellowship from the European Commission, Brussels,
References (89)
Frugivory and seed dispersal by vertebrates in tropical and subtropical Asia: an update
Glob. Ecol. Conserv.
(2017)- et al.
Avian assemblages in native Acacia and alien Prosopis drainage line woodland in the Kalahari, South Africa
J. Arid Environ.
(2002) Non-specialized frugivores as key seed dispersers in dry disturbed environments: an example with a generalist neotropical mesocarnivore
J. Arid Environ.
(2019)Seed dispersal by fruit-eating birds and mammals
- et al.
Red fox (Vulpes vulpes L.) favour seed dispersal, germination and seedling survival of Mediterranean hackberry (Celtis australis L.)
Acta Oecol.
(2006) - et al.
Social organization, survival, and dispersal of cape foxes (Vulpes chama) in South Africa
Mamm. Biol.
(2014) - et al.
Ecological relationships of black-footed cats (Felis nigripes) and sympatric canids in South Africa
Mamm. Biol.
(2015) - et al.
The bat-eared fox: a dietary specialist?
Mamm. Biol.
(2011) - et al.
Seeds dispersed in dung of insectivores and herbivores in semi-arid southern Africa
J. Arid Environ.
(2001) - et al.
Patterns of seed occurrence in corsac and red fox diets in Mongolia
J. Arid Environ.
(2009)