The Potential for Birds to Disperse the Seeds of Acacia Cyclops, an Invasive Alien Plant in South Africa

Ibis (2015), 157, 449–458 The potential for birds to disperse the seeds of Acacia cyclops, an invasive alien plant in South Africa † THABISO M. MOKOTJOMELA,1* JOHN H. HOFFMANN1 & COLLEEN T. DOWNS2 1Department of Biological Sciences, University of Cape Town, Private Bag X3, Rondebosch 7701, South Africa 2DST-NRF Centre for Invasion Biology, School of Life Sciences, University of KwaZulu-Natal, Scottsville 3209, Pietermaritzburg, South Africa Rooikrans Acacia cyclops is an aggressive invasive tree that threatens natural resources in South Africa. The seeds of A. cyclops have a prominent aril which attracts birds that ingest the seeds and disperse them endozoochorously. Two biological control agents, a Seed Weevil Melanterius servulus and a Flower-galling Midge Dasineura dielsi, were released on A. cyclops in 1991 and 2002, respectively. Together these agents have substantially reduced seed production and generally far lower numbers of seeds are now available to birds. A con- sequence of this transition from historically bounteous quantities of seeds to scanty seed availability is that birds may no longer associate with the trees and seed dispersal may be disproportionately reduced. To assess whether this has happened, seed attrition was mea- sured by comparing the amount of seeds that disappeared from two groups of branches, one available to birds and the other enclosed in bird netting. Other types of granivores (mainly field mice) were excluded from both groups of branches with a plastic funnel placed around the stems. Mature seeds were also harvested and fed to caged bird species to determine gut retention times and germination rates of ingested seeds. Attrition rates of seeds showed that birds continue to remove seeds but that only a proportion of the crop is taken. Only two frugivorous species (Knysna Turaco Tauraco corythaix and Red-winged Starling Onychognathus morio) and two granivorous species (Red-eyed Dove Streptopelia semitorquata and Laughing Dove Streptopelia sengalensis) ingested A. cyclops seeds during feeding trials. Ingestion by birds enhanced seed germination except for those ingested by Laughing Doves. There were no apparent effects of length of gut passage time and avian body size on seed germination rates. Despite the diminished seed resource due to biological control agents, birds continue to disperse A. cyclops seeds. Keywords: bird, dispersal distance, germination rate, gut-passage time, invasive trees. The contribution that dispersers make to the indicate that quantity, rather than quality, is more future reproduction of plants is determined by two influential in seed dispersal effectiveness (Schupp components, the product of quantity (number) 1993). At present there is a limited understanding and quality (probability of becoming a new adult of seed dispersal effectiveness in general (Wang & plant) of seeds dispersed (Schupp 1993, Traveset Smith 2002, Nathan 2007, Mokotjomela 2012), et al. 2001, Schupp et al. 2010). Many studies with only one thorough study undertaken to date that focused on Australian tropical forests (Dennis †Present address: Global Change and Sustainability Research & Westcott 2006). Institute, University of the Witwatersrand, Private Bag 3, Wits Birds are important dispersers of seeds (Howe 2050, Johannesburg, South Africa. & Smallwood 1982, Jordano 2000, Schupp et al. 2010), with seed mortality and dispersal distances *Corresponding author. fl Emails: [email protected], mokotjomelat@yahoo. both likely to be in uenced by gut passage time in co.uk birds (Nathan 2007, Schurr et al. 2009, Tsoar © 2015 British Ornithologists’ Union 450 T. M. Mokotjomela, J. H. Hoffman & C. T. Downs et al. 2011, Mokotjomela et al. 2013a). Benefits of African Mediterranean climate region, where inva- avian endozoochory include dormancy release and sive alien trees constitute a major threat to native enhanced germination (Howe & Smallwood 1982, plant communities (Richardson et al. 1992). Pre- Schupp et al. 2010), especially where there is vec- dominant among these invasive trees are several tor-specificity (Traveset et al. 2001). Although ger- Australian Acacia species which have been tar- mination may be enhanced by passage through a geted with biological control using insect herbi- bird’s gut, it may also remain unchanged or even vores that destroy the flowers or developing seeds be suppressed (Traveset 1998, LaFleur et al. 2009, (Impson et al. 2011). One of these is Acacia Jordaan et al. 2011, Mokotjomela 2012, Chama cyclops, which now has two biological control et al. 2013). Movement over long distances influ- agents in South Africa, a Seed Weevil Melanterius ences dispersal quality by reducing intraspecific servulus and a Flower-galling Fly Dasineura dielsi, competition and seed predation, which are gener- both of which substantially reduce overall levels of ally higher close to the source (Howe & Small- seed production (Impson et al. 2009, 2011, Moran wood 1982), by opening genetic links between et al. 2013). disconnected plant communities (Van Der Pijl Birds have historically been implicated as major 1982, Nathan et al. 2008, Schurr et al. 2009, dispersal vectors driving the invasion of A. cyclops Schupp et al. 2010) and by facilitating the forma- in South Africa (Glyphis et al. 1981, Knight 1988, tion of new self-sustaining populations in different Underhill & Hofmeyr 2007, Mokotjomela & Hoff- landscapes (Sakai et al. 2001, Nathan et al. 2008). mann 2013). Of the approximately 70 Australian Although some aspects of avian seed dispersal Acacia species that have been introduced into have been studied thoroughly (Knight 1988, South Africa, predominantly during the 19th Cowling et al. 1997, Jordaan et al. 2011, Mokotjo- century, at least 13 are recognized as invasive mela et al. 2013a), quantifying patterns of seed (Henderson 2001, Richardson et al. 2011, Van dispersal distances remains a challenge (Nathan Wilgen et al. 2011). Acacia cyclops was introduced 2001, Schurr et al. 2009). A traditional seed- into southern Africa in 1835, primarily for stabil- centred approach to understanding dispersal has ization of sand dunes in the southwestern Cape inferred dispersal distances from fruit/seed mor- (Shaughnessy 1980). It has since successfully natu- phology and the potential pool of consumers (Hig- ralized and invaded coastal regions across the gins et al. 2003), with more recent studies southern Cape (Henderson 2001). The prolifera- continuing to emphasize seed recovery location as tion of A. cyclops is ascribed to its widespread the only means of determining seed dispersal dis- propagation as a source of fuel wood for domestic tances (e.g. Scott & Batchelor 2014). This and small-scale commercial purposes (Richardson approach provides limited understanding of rare et al. 2011, Van Wilgen et al. 2011) and to its long-distance dispersal events when compared prolific seed production (Milton & Hall 1981, with a contemporary vector-based approach that Impson et al. 2009). Each seed has a prominent utilizes vector characteristics and behaviour to reddish-orange aril that attracts vertebrates, espe- determine seed dispersal distances (Nathan et al. cially birds, which consume and pass the indigest- 2008, Schurr et al. 2009, Tsoar et al. 2011). A ible seeds, thereby enhancing the spread of the main assumption with this approach is that dis- plant (Glyphis et al. 1981, Underhill & Hofmeyr persal distance is positively correlated with the 2007, Mokotjomela & Hoffmann 2013). The seeds body size of a vector (Schurr et al. 2009, Tsoar are also buried in accumulations by ants (Holmes et al. 2011, Mokotjomela et al. 2013a). However, 1990) and possibly seed-hoarding rodents (Midgley dispersal distances are also influenced by spatial & Anderson 2005, Rusch 2011). distributions of fruit or seed resources (Mokotjo- Among the bird species documented as feeding mela et al. 2013a). on the seeds of A. cyclops (Glyphis et al. 1981), at Knowledge of bird-mediated seed dispersal can least one, the Red-winged Starling Onychognathus help in predicting future plant distribution ranges morio, has been shown to enhance seed germina- (Nathan et al. 2008, Tsoar et al. 2011, Mokotjo- tion rates (Impson 2005). Impson (2005) also mela et al. 2013a), and in screening the potential demonstrated that while high levels of feeding invasiveness of both established and emerging alien damage by the native alydid bugs Zubulius spp. plants (Tucker & Richardson 1995, Nel et al. reduced seed viability, moderate levels of damage 2004). This is certainly pertinent in the South increased germination rates of seeds ingested and © 2015 British Ornithologists’ Union Avian endozoochory in Acacia cyclops 451 passed by birds. Nevertheless, the impact of other from cool drink (soda) bottles around the proximal factors, such as microbes and arthropods, on seed portion of the stem. All branches were chosen on viability and germination rates has generally been trees of approximately equal height: 4.1 Æ 0.3 m overlooked in studies investigating endozoochorous (mean Æ se) at Koeberg Nature Reserve and seed dispersal (Fricke et al. 2013). 5.6 Æ 0.3 m at Langebaanweg. Total seed produc- The aim of this study was to assess whether tion on each tagged branch was calculated by birds continue to consume seeds of A. cyclops at counting the number of seed-bearing pods and high levels in plant populations when seed produc- multiplying this value by the average number of tion is both curbed and erratic due to biological seeds per pod (8.7 Æ 0.4 seeds). Seed removal

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