South African Journal of Botany 86 (2013) 73–78

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South African Journal of Botany

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Frugivorous birds visit fruits of emerging alien species more frequently than those of native shrub species in the South African Mediterranean climate region

T.M. Mokotjomela a,b,⁎, C.F. Musil a, K.J. Esler b a Climate Change and Bio-Adaptation Division, Private Bag X7, Claremont 7735, South b Department of Conservation Ecology and Entomology & Centre for Invasion Biology, Stellenbosch University, Private Bag X1, Matieland 7602, article info abstract

Article history: We compared daily visitation frequency indices by 4 large (>150 g), 7 medium-size (50–150 g), 5 small Received 14 November 2012 (30–50 g) and 8 and tiny (b30 g) frugivorous bird species on fleshy fruits of two native (Olea Received in revised form 31 January 2013 europaea subsp. africana and Chrysanthemoides monilifera subsp. monilifera), two established alien shrubs Accepted 6 February 2013 ( mauritianum and Lantana camara) and two emerging alien shrubs (Myoporum tenuifolium and Available online 16 March 2013 Pittosporum undulatum) at nine different sites in the Cape Floristic Region. Large, medium-size and tiny fi Edited by J Van Staden birds as groups displayed signi cantly higher visitation frequency indices on fruits of both emerging alien shrub species than the other shrub species. Small birds as a group displayed insignificantly different visitation Keywords: frequency indices on fruits of both emerging and established alien shrub species but significantly higher Bird species richness visitation frequency indices on fruits of both emerging and established alien shrub species than on fruits of Bird body mass the native shrub species. However, there were significant differences in foraging frequency indices of the Established alien bird species included within each of these body size groups on fruits of the different shrub species. Among Emerging alien plants the large birds, Columba guinea and among the medium size birds Sturnus vulgaris, Streptopelia senegalensis, Native plants Turdus olivaceus and Onychognathus morio all exhibited significantly higher visitation frequency indices on Bird visitation frequency fruits of both emerging alien shrub species than on fruits of the other shrub species. These findings indicate that alien control measures should be focused on eradicating localised populations of emerging aliens to limit preferential consumption of their fruits by birds and consequent dispersal of their seeds that germi- nate readily into natural areas. © 2013 SAAB. Published by Elsevier B.V. All rights reserved.

1. Introduction thicket and afromontane forests, 28% of true fynbos shrubs and 46% of renosterveld shrubs rely on birds for dispersal of their seed Globally, many fleshy-fruited plants rely on birds and other ver- (Le Maitre and Midgley, 1992). tebrates for dispersal of their seeds (Howe and Smallwood, 1982; Habitat disturbance and importation of alien plants for horticul- Jordano, 2000). It has been estimated that vertebrates disperse about tural purposes has resulted in the invasion of natural habitats by 90% of and shrubs in tropical regions, 50% in neo-tropical regions, fleshy-fruited alien plants in many global ecosystems (Rejmanek, 20–60% in Mediterranean-climate regions and about 40% in temperate 1996; Richardson and Rejmánek, 2011). This is assisted by bird- regions with birds being the predominant vertebrate dispersal agents mediated seed dispersal of fleshy-fruited invasive alien plants (Willson et al., 1989; Jordano, 2000). The different proportions are which, is well-documented globally (Traveset and Richardson, 2011; associated with variation in fruit production in different regions Richardson and Rejmánek, 2011). It has been reported that birds dis- although there are some overlaps between sub-regions and regions perse 25% of the 199 globally representative invasive species (Cronk (Jordano, 2000; Herrera, 2002). According to Knight and Siegfried and Fuller, 1995), 43% of the invasive alien trees and 61% of invasive (1983), 52% of the 1340 species of indigenous angiosperm trees alien shrubs in 15 distinct global geographical regions (Richardson in southern Africa produce fleshy fruits with 23% predominantly and Rejmánek, 2011). The extra-tropical regions such as the temper- relying on birds for dispersal of their seeds. In the South African ate and Mediterranean-climate regions, except those in the Mediter- Mediterranean-climate region, it has been estimated that 80% of the ranean Basin, seem more vulnerable to invasion by alien plants fleshy-fruited woody species in succulent karroid scrubland, dune (Rejmanek, 1996; Rejmanek et al., 2005) due to massive habitat frag- mentation (Herrera, 1995). Presently, the Mediterranean-climate region of South Africa ranks second to in terms of numbers ⁎ Corresponding author at: Climate Change and Bio-Adaptation Division, Private Bag fl X7, Claremont 7735, South Africa. Tel.: +27 733 246118; fax: +27 21 7976903. of invasive eshy-fruited woody alien species (Richardson and E-mail address: [email protected] (T.M. Mokotjomela). Rejmánek, 2011), many of which possess fruit attributes attractive

0254-6299/$ – see front matter © 2013 SAAB. Published by Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.sajb.2013.02.004 74 T.M. Mokotjomela et al. / South African Journal of Botany 86 (2013) 73–78 to birds (Vittoz and Engler, 2007). Initial assessments indicate that 51 44.84 S 18° 23′ 55.49 E), Constantia (33° 49′ 30.26 S 18°47′ 37.64 E), of the 1698 alien plant species introduced into southern Africa possess Silvermine (37° 41′ 41.20 N 024° 01′ 09.48 E), Kalk Bay (34° 07′ 40 S fleshy fruits dispersed by birds (Knight, 1986) with these numbers in- 18° 26′ 54 E), Simons Town (34°16′22.30 S 18°42′94.20 E) all located creasing (Richardson and Rejmánek, 2011). It is presumed that migra- on Peninsula Granite Fynbos; Paarl (33° 45′ 27.22 S 19° 01′ 32.86 E) lo- tion of about 63 of the 224 terrestrial bird species present in southern cated on Swartland Shale Renosterveld; Franshoek ( 33° 53′ 57.6 S 19° Africa into the Mediterranean-climate region of South Africa (Cowling 06′ 10.5 E) located on Boland Granite Fynbos; Swellendam (34° 02′ and Richardson, 1995) has been associated with the introduction for 27.09 S 20° 33′ 03.06 E) located on Breede Shale Renosterveld and commercial, horticultural and forestry purposes of alien trees and Hermanus (34° 24′ 01.06 S 19° 12′ 42.49 E) located on Overberg Sand- shrubs with fleshy fruit displays (Richardson and Rejmánek, 2011). stone Fynbos. Two native shrub species, two established alien shrub These migrant birds have presumably contributed to the expansion species and two emerging alien shrub species with overlapping fruiting of alien plant infestations in the Cape Floristic Region through dis- periods (Knight, 1988; Van Wyk and Van Wyk, 1997)anddistribution persal of their seeds (Cowling and Richardson, 1995; Richardson and ranges were selected for comparisons of bird visitation frequencies Van Wilgen, 2004). This is typified by the reported dispersal of on their fleshy fruits. Distribution ranges were based on records Acacia cyclops seeds by the Onychognathus morio (Glyphis et al., extracted from PRECIS (Germishuizen et al., 2006), ACKDAT (Mucina 1981; Richardson et al., 1992). Although frugivorous birds are effec- and Rutherford, 2006)andSAPIA(Henderson, 2011) databases. The tive seed dispersers of fleshy-fruited alien plants most probably native shrubs comprised Chrysanthemoides monilifera subsp. monilifera owing to their occasionally nutritious fruits (Jordaan and Downs, (L) Norlindh. (Asteraceae) and Olea europaea subsp. africana Mill 2012; Mokotjomela et al., 2013), recent studies generally suggest (Oleaceae), commonly referred to as O. africana.Theestablishedalien that passage of seeds through guts of these frugivores does not in- shrubs comprised L. camara L (Verbenaceae) and S. mauritianum Scopoli crease germination of invasive alien plants (e.g. Solanum mauritianum, () and the emerging alien shrubs comprised Myoporum Cinnamomum camphora, Lantana camara and Psidium guajava)in tenuifolium Auct (Myoporaceae) and Pittosporum undulatum Vent South Africa yet their removal of fruit pulp does (Jordaan et al., (Pittosporaceae). C. monilifera, O. africana, L. camara and M. tenuifolium 2011). In this way, a major role of the avian frugivores remains as produce small fruits (drupes) each containing a single nutlet (seed), dispersal of seeds to distant micro sites of which Sakai et al. (2001) in- except L. camara whose drupes contain two nutlets, the fruits turning dicated that this leads to establishment of multiple population foci purplish or black when ripe. In contrast, S. mauritianum produces clus- that rapidly expand to homogenise the environment. Nevertheless, ters of yellow fruit, about 10 mm in diameter (Henderson, 2001), there are no comparative studies on the frequency of visitations by dif- each containing up to 193 seeds (Witkowski and Garner, 2008)and ferent frugivorous bird species on fruits of alien and indigenous plants P. undulatum produces globe-shaped fruit capsules about 16 mm long, in the Cape Floristic Region, a global biodiversity hotspot (Myers et al., each containing 20–40 sticky orange seeds ingested by frugivores 2000) characterised by its exceptionally high species richness (9086 (Binggeli et al., 1998). species in an area of 87,892 km2) and high fraction (68.2%) of endemic species (Cowling et al., 1989). The foraging visitation frequency of 2.2. Bird species and visitation frequencies birds on fruits is associated with seed dispersal potential with high visitation indicative of greater chances of seeds being removed and Bird observations were restricted to the peak fruiting season dispersed (Vazquez et al., 2005; Schupp et al., 2010; Mokotjomela, (i.e. autumn to spring of 2009 and 2010) of the native, established 2012). Past studies have merely identified individual species of birds alien and emerging alien shrub species and was done daily to 3 h observed foraging on fruits of alien plants (Glyphis et al., 1981; early morning and 3 h late afternoon periods of maximum bird activity Knight, 1988; Underhill and Hofmeyr, 2007) and how these related (La Rosa et al., 1985; Bibby et al., 2000). Bird species identifications were to fruiting displays and fruiting phenology (Knight, 1988). aided by descriptions and keys presented in Sinclair and Ryan (2003) Frugivorous birds concentrate their activities where fruit resources and Hockey et al. (2005). Measurements of bird foraging activity on are most visible and abundant (Saracco et al., 2005; Blendinger et al., randomly selected reproductively mature individuals of each shrub spe- 2008; Aslan and Rejmánek, 2012; Mokotjomela et al., 2013) and cies at each site were performed with binoculars (8×42 magnification) consequently alien plants with colourful fruit displays, high fruit at a distance of about 30 m from each shrub, and simultaneously abundance and nutritional content (Saracco et al., 2005; Carlo et al., recorded with a digital camcorder (Kodak C813: 8.2 megapixel, ISO 2007; Jordaan and Downs, 2012) may be presumed to attract a greater 1250, digital IS) for a permanent photographic record (Spiegel and diversity of frugivorous bird species more frequently than fruits of Nathan, 2007). Five days of bird observations were conducted on each native plants. Also, the established stands, widely distributed, high of the six shrub species, the fruit crop sizes of the individual shrub spe- density populations of alien plants that offer numerous perching cies differing between sites and consequently included as a source of opportunities and food resources for foraging birds, especially in the variation. Only one shrub species was monitored at a time over each Cape Floristic Region (Knight, 1988; Manders and Richardson, 1992; daily observation period at each site. At each site, all frugivorous bird Mokotjomela et al., 2013), may be presumed to be more attractive species (Hockey et al., 2005) that were observed actively consuming to frugivorous birds than populations of emerging aliens with limited fruits of the native, established alien and emerging alien shrub species distributions. In view of these presumptions, we predicted that fleshy were recorded. Each visitation comprised an arrival and departure fruits of established alien shrub species will be visited more frequently time of an individual foraging bird species, irrespective of visitation by frugivorous birds than those of emerging alien and native shrub length, with the numbers of recorded visitations for each frugivorous species. bird species summed for each 6-h daily observation period.

2. Methods and materials 2.3. Data synthesis and statistical analysis

2.1. Study sites and shrub species selection Recorded foraging bird species were classified into four body mass groups defined by Dennis and Westcott (2007), namely large birds There were nine study sites located in different natural vegetation (>150 g), medium size birds (50–150 g), small birds (30–50 g) and units (Mucina and Rutherford, 2006) within the Cape Floristic Region, tiny birds (b30 g). A nested analysis of variance (bird species nested each comprising mixed populations of native and alien shrubs within each shrub species) tested for differences in daily visitation bearing fleshy fruits frequently consumed by local frugivorous birds frequencies by birds of different body mass and species on fruits of (Richardson and Fraser, 1995). The sites comprised Hout Bay (34° 00′ the native, established alien and emerging alien shrub species. Also, T.M. Mokotjomela et al. / South African Journal of Botany 86 (2013) 73–78 75

of the native, established alien and emerging alien shrubs (Fig. 1). However, the total numbers of bird species observed foraging on fruits of both native shrubs over all sites were higher than the total numbers observed foraging on fruits of the established alien and emerging alien shrubs (Fig. 1). Large, medium-size and tiny birds as groups displayed significantly higher (P≤0.001) visitation frequency indices on fruits of both emerging alien shrub species than the other shrub species (Table 1). Small birds as a group displayed in- significantly (P≥0.05) different visitation frequency indices on fruits of both emerging and established alien shrub species but signifi- cantly (P≤0.01) higher visitation frequency indices on fruits of both emerging and established alien shrub species than on fruits of the native shrub species (Table 1). However, there were significant (P≤0.05) differences in foraging frequency indices of the bird species included within each of these size groups on fruits of the different shrub species. Among the large Fig. 1. Average numbers of frugivorous bird species per site±standard errors foraging fi ≤ on fruits of native (C. monilifera-C. mon and O. africana-O. afr), established alien birds, only Columba guinea displayed a signi cantly (P 0.001) higher (L. camara-L. cam and S. mauritianum-S. maur) and emerging alien (M. tenuifolium- visitation frequency index on fruits of both the emerging alien shrub M. ten and P. undulatum-M.) shrub species. species than the other shrub species. Among the other large birds, Streptopelia capicola exhibited a significantly (P≤0.05) higher visita- an analysis of variance tested for differences in the average numbers tion frequency index on fruits of the emerging alien M. tenuifolium of bird species per site foraging on fruits of the individual shrub spe- only and Columba arquatrix exhibited a significantly (P≤0.05) higher cies included in native, established alien and emerging alien shrub visitation frequency index on fruits of both the emerging alien groups. Significantly different means were separated with a Duncan's M. tenuifolium and the established alien S. mauritianum than on multiple range test. fruits of the other shrub species (Table 1). Among the medium size birds, four species, namely Sturnus vulgaris, Streptopelia senegalensis, 3. Results Turdus olivaceus and Onychognathus morio all exhibited significantly (P≤0.05) higher visitation frequency indices on fruits of both There was no statistical significant (P≥0.05) difference in the emerging alien shrub species than on fruits of the other shrub species average numbers of bird species per site observed foraging on fruits (Table 1). Among the other medium-size birds, Laniarius ferrugineus

Table 1 Variance (F) ratios and mean daily visitation frequency indices±standard errors for frugivorous bird species of different body mass foraging on fruits of different shrubs. Frequencies ⁎ ⁎⁎ ⁎⁎⁎ in bold with different letters are significantly greater at P≤0.05; P≤0.01; P≤0.001.

Mass class/scientific name Nested ANOVA Native shrubs Established alien shrubs Emerging alien shrubs

Shrub Bird (shrub) C. monilifera O. africana L. camara S. mauritianum M. tenuifolium P. undulatum

⁎⁎⁎ ⁎⁎⁎ a a ab bc d cd All birds F5,558 =19.66 F96,558 =1.68 1.21±0.24 1.76±0.34 3.08±0.67 5.32±1.09 7.50±0.62 7.05±1.04 ⁎⁎⁎ a a a ab b c Large birds: >150 g F5,93 =4.94 F12,93 =1.15 1.19±0.45 1.31±0.51 1.17±0.47 5.00±2.57 7.78±1.57 22.00±0.34 ⁎⁎⁎ ⁎⁎⁎ a a a a b b Medium birds: 50–150 g F5,197 =13.91 F32,197 =2.23 1.04±0.31 1.75±0.53 2.13±0.68 2.33±1.01 7.79±0.74 6.36±1.13 ⁎⁎ a a ab b b ab Small birds: 30–50 g F5,85 =3.95 F11,85 =0.98 1.21±0.49 1.67±0.89 4.38±1.44 9.00±2.38 7.00±1.62 4.67±1.43 ⁎⁎⁎ ⁎⁎ a a ab b b b Tiny birds: b30 g F5,180 =4.39 F23,180 =2.22 1.38±0.55 2.06±0.66 5.31±2.06 8.19±2.19 7.21±1.29 7.91±2.16 Large bird species Columba arquatrix African olive-pigeon 1.75±1.18a 0.50±0.50a 1.25±0.95a 15.00±4.74b 9.33±3.33b 0.00±0.04a Streptopelia capicola Cape turtledove 2.00±0.91a 3.75±1.44a 1.00±1.00a 0.00±0.00a 9.33±2.40b 0.00±0.00a Columba guinea Speckled pigeon 1.00±1.00a 0.75±0.48a 1.25±0.75a 0.00±0.00a 7.48±1.84b 22.00±0.34c Streptopelia semitorquata Red-eyed dove 0.00±0.00a 0.25±0.25a 0.00±0.00a 0.00±0.00a 0.00±0.00a 0.00±0.00a Medium bird species Sturnus vulgaris Common starling 0.00±0.00a 0.75±0.75a 0.00±0.00a 0.00±0.00a 10.91±1.84b 8.67±6.67b Streptopelia senegalensis Laughing dove 0.00±0.00a 0.00±0.00a 0.00±0.00a 0.00±0.00a 5.00±3.00b 9.50±2.87b Turdus olivaceus Olive thrush 1.25±0.63a 1.25±0.75a 2.50±1.04a 1.50±0.87a 8.00±3.12b 4.00±0.63b Urocolius indicus Red-faced mousebird 1.75±1.18a 0.00±0.00a 0.00±0.00a 0.00±0.00a 0.00±0.00a 0.00±0.00a Onychognathus morio Red-winged starling 1.75±1.18a 2.75±1.55a 2.00±0.82a 0.00±0.00a 10.83±1.93b 8.00±2.97b Laniarius ferrugineus Southern boubou 1.75±1.03a 2.00±1.41a 1.50±1.19a 0.25±0.25a 3.33±1.33a 8.40±2.99b Colius striatus Speckled mousebird 0.75±0.75a 5.50±2.10a 6.75±2.75a 12.25±2.39b 6.29±0.79a 6.00±0.00a Small bird species Pycnonotus capensis 4.25±2.36a 5.00±5.00a 7.25 ±1.65ab 11.50±2.72b 8.00±1.99ab 4.67±1.43a Ploceus capensis Cape weaver 1.00±0.57a 0.25±0.25a 0.00±0.00a 0.00±0.00a 0.00±0.00a 0.00±0.00a Andropadus importunus Sombre bulbul 0.00±0.00a 0.25±0.25a 0.00±0.00a 0.00±0.00a 0.00±0.00a 0.00±0.00a Ploceus velatus Southern masked-weaver 1.50±0.87a 4.00±1.78ab 1.50±1.19a 6.50±3.84b 3.20±0.80ab 0.00±0.00a Tchagra tchagra Southern tchagra 0.50±0.50a 0.50±0.50a 0.00±0.00a 0.00±0.00a 0.00±0.00a 0.00±0.00a Tiny bird species Emberiza capensis Cape bunting 0.00±0.00a 1.75±1.03a 0.00±0.00a 0.00±0.00a 0.00±0.00a 0.00±0.00a Serinus canicollis Cape canary 0.75±0.25a 2.75±0.75bc 2.00±0.92ab 4.50±1.04cd 0.00±0.00a 5.50±1.50d Cossypha caffra Cape robin-chat 2.25±1.11ab 1.25±0.95a 2.25±0.85ab 1.50±0.64a 5.86±1.87b 0.00±0.00a Zosterops pallidus Cape white-eye 7.00±2.97a 9.25±3.25a 17.0±4.65ab 26.75±3.04b 7.59±1.57a 8.86±3.52a Sigelus silens Fiscal flycatcher 0.00±0.00a 0.25±0.25a 0.00±0.00a 0.00±0.00a 0.00±0.00a 0.00±0.00a Parus afer Grey tit 0.00±0.00a 0.00±0.00a 0.00±0.00a 0.00±0.00a 0.00±0.00a 0.00±0.00a Passer domesticus House sparrow 0.00±0.00a 1.25±0.75a 0.00±0.00a 0.00±0.00a 0.00±0.00a 7.00±3.69b Crithagra flaviventris Yellow canary 1.00±1.00a 0.00±0.00a 0.00±0.00a 0.00±0.00a 0.00±0.00a 0.00±0.00a Total bird species 16 20 12 9 13 11 76 T.M. Mokotjomela et al. / South African Journal of Botany 86 (2013) 73–78 exhibited a significantly (P≤0.05) higher visitation frequency index of established alien trees are often less rich in plant species and on fruits of the emerging alien P. undulatum only and Colius striatus fruit resources, which in Spanish Mediterranean scrubland were ob- exhibited a significantly (P≤0.05) higher visitation frequency index served to attract fewer bird species (De La Montana et al., 2006). on fruits of only the established alien S. mauritianum than on fruits This feature also evident in this study where slightly fewer bird spe- of the other shrub species (Table 1). Among the tiny birds, Cossypha cies on average were observed visiting fruits of the established alien caffra displayed a significantly (P≤0.05) higher visitation frequency than emerging alien shrub species. Another potential explanation index on fruits of the emerging alien M. tenuifolium only and Passer for the significantly higher visitation frequency indices displayed domesticus and Serinus canicollis have significantly (P≤0.05) higher by most large and medium-size birds as well as some tiny birds on visitation frequency indices only on fruits of only the emerging fruits of the two emerging alien species is the opportunistic foraging alien P. undulatum than the other shrub species (Table 1). The tiny behaviour displayed by frugivorous birds on fruits of novel alien Zosterops pallidus differed in exhibiting a significantly (P≤0.05) plants (Mandon-Dalger et al., 2004; LaFleur et al., 2007; Kueffer higher visitation frequency index on fruits of only the established et al., 2009). Many foraging birds tend to prefer new fruits which alien S. mauritianum than the other shrub species (Table 1). Among are often more attractive than their customary fruits (Knight, 1986; the small birds, Ploceus velatus displayed a significantly (P≤0.001) Lafleur et al., 2007) as they provide a means of maximising energy higher visitation frequency on fruits of the established alien acquisition (Kueffer et al., 2009; Gosper and Vivian-Smith, 2010). S. mauritianum than the other shrub species whereas Pycnonotus Also, local frugivorous birds in the Cape Floristic Region display a capensis displayed insignificantly (P≥0.05) different visitation fre- greater preference for alien fruits where large scale habitat modifica- quency indices on fruits of both the emerging alien M. tenuifolium tion has reduced the variety of native fruits (Oatley, 1984). Therefore, and the established aliens S. mauritianum and L. camara, but displayed the close association of birds with human settlements which are rich a significantly (P≤0.05) higher visitation frequency index on fruits of in emerging alien fruit resources (Cowling and Richardson, 1995; only the established alien S. mauritianum than on fruits of the native Reichard et al., 2001; Aslan and Rejmánek, 2010) and the relatively shrub species (Table 1). close proximity of several of the study sites possessing emerging aliens to urban areas may explain the observed higher visitation fre- 4. Discussion quency indices by frugivorous birds on fruits of the emerging alien group. The quantity and variety of seeds dispersed by birds have been There was no clear explanation for the significantly higher visita- positively correlated with frugivore bird species richness (Garcia tion frequency indices displayed by several different size bird species, and Martinez, 2012), an important determinant of population dy- such as the large S. capicola and C. arquatrix, the medium-size namics in diverse plant communities (Dennis and Westcott, 2007). S. vulgaris, O. morio and T. olivaceus and C. caffra on fruits of the Although fleshy fruits of alien plants are an important supplemental emerging alien M. tenuifolium. One possible explanation is the heavy fruit source for native avian frugivore species (Mokotjomela et al., and continuous year round fruit production by M. tenuifolium occur- 2009; Gleditsch and Carlo, 2010; Jordaan et al., 2011), we observed ring in areas of low vegetation density and high habitat heterogeneity no statistically significant difference in the average numbers of bird which experience frequent visitations by frugivorous birds. This species per site observed foraging on fruits of the native, established suggestion was supported by previous reports of the attraction of alien and emerging alien shrub species in this study. This is possibly the C. caffra to the dense thickets of natural vegetation (Manders a consequence of the relatively few endemic frugivorous bird species and Richardson, 1992) and thus true for thick stands of M. tenuifolium. and fleshy fruit resources in the South African Mediterranean climate Also it has been reported that heavily fruiting Sambucus nigra attracts region (Cody, 1983). large flocks of the European starling (S. vulgaris) in In contrast, several of the large, medium-size and tiny bird species (Williams and Karl, 1996) and the heavily fruiting Juniperus ashei displayed significantly higher visitation frequency indices on fruits attracts large flocks of the American robin (Turdus migratorius)in of either one or both of the two emerging alien species than the Texas (Chavez-Ramirez and Slack, 1994). Furthermore, bird foraging other shrub species. A meta-analysis of published data and fruit behaviour profiles are shaped by factors such as predation and choice-tests using caged birds (Aslan and Rejmánek, 2012) concluded competition for limited fruit resources (Knight, 1988; Manders and that bird preferences for alien fruits was due to their greater visibility Richardson, 1992). As a consequence, birds tend to congregate on and attractiveness. This premise may have potentially applied to the and forage on fruits of less known emerging shrubs rather than large conspicuous orange coloured fruits of P. undulatum (Binggeli recognised established alien and native shrubs species where there et al., 1998) but not necessarily to the smaller purplish coloured is a higher likely interference from other bird species thereby fruits of M. tenuifolium (Bornhorst, 1996) whose colouring and archi- minimising their exposure to predators and competition for available tecture was similar to the fruits produced by the two native shrub fruit resources (Martin, 1985; Saracco et al., 2004). species C. monilifera and O. africana (Scott, 1996; Rey and Alcantara, The high visitation frequency indices displayed by several different 2000) and the established alien shrub species L. camara (Day et al., size bird species, such as the large C. arquatrix, the medium-size 2003). P. undulatum fruits contain numerous sticky orange seeds C. striatus, the small P. velatus and P. capensis and the tiny Z. pallidus likely attractive to granivorous birds such as the large C. guinea, the on fruits of the established alien S. mauritianum seemed a likely conse- medium-size S. senegalensis, the tiny P. domesticus and S. canicollis quence of S. mauritianum's high fruit mass and energy content in which all displayed significantly higher visitation frequency indices South Africa (Jordaan et al., 2011; Mokotjomela et al., 2013) which on fruits of the emerging alien P. undulatum. Also, it has been reported have been reported to be directly correlated with measured quantities that frugivorous birds do prefer foraging at the margins of forest of fruit pulp consumed by birds (Johnson et al., 1985). Also, since gaps (Restrepo et al., 1999; Carlo et al., 2007) where emerging alien frugivorous birds tend to vary their diet with arthropods (Jordano, trees are more prolific in the Cape Floristic Region (Bond, 1995). 1988) which are abundant on alien plants both in the South African The edges of forest gaps are characterised by diverse fruit resources Mediterranean climate region (Proches et al., 2008), as well as in and high habitat heterogeneity which are targeted by a large array southeast Texas (Hartley et al., 2010), the diverse floral and faunal of bird species during breeding seasons (Restrepo et al., 1999; De resources associated with S. mauritianum's continuous fruit produc- La Montana et al., 2006), and consequently fruiting plants established tion may have also contributed to the high bird visitation frequency in these habitats experience frequent visitations by frugivorous birds. indices. Such habitats also preferred by bird species in Spanish Mediterranean In conclusion, this study's findings indicate that the eradication woodlands (De La Montana et al., 2006). In contrast, dense stands of emerging aliens, whose impacts on natural habitats are likely less T.M. Mokotjomela et al. / South African Journal of Botany 86 (2013) 73–78 77 severe during early stages of invasion (Nel et al., 2004; Buckley et al., De La Montana, E., Rey-Benayas, J.M., Carrascal, L.M., 2006. Response of bird communi- ties to silvicultural thinning of Mediterranean Maquis. Journal of Applied Ecology 2006), should be prioritised (Aslan and Rejmánek, 2010). Also, the 43, 651–659. suppression of populations of alien birds such as the S. vulgaris Dennis, A.J., Westcott, D.A., 2007. Estimating dispersal kernels produced by diverse and the P. domesticus require prioritisation, since several studies community of vertebrates. In: Dennis, A.J., Schupp, E.W., Green, R.J., Westcott, D.A. 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South African Botanical Diversity Network report No. 41. partly accelerated by the presence of alien mutualistic partners SABONET, Pretoria. Gleditsch, J.M., Carlo, T.A., 2010. Fruit quantity of invasive shrubs predicts the abun- (Mandon-Dalger et al., 2004; Traveset and Richardson, 2011). How- dance of common native avian frugivores in central Pennsylvania. Diversity and ever, alien birds have also been reported to be instrumental in the Distributions 17, 244–253. dispersal of seeds of native plants where native avian dispersers are Glyphis, P.J., Milton, J.S., Siegfried, R.W., 1981. Dispersal of Acacia cyclops by birds. Oecologia 48, 138–141. absent (Foster and Robinson, 2007; Kawakami et al., 2009). Conse- Gosper, C.R., Vivian-Smith, G., 2009. Approaches to selecting native plant replacements quently, fleshy-fruited alien plant eradication programmes should for fleshy-fruited invasive species. 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