Fig Wasps (Hymenoptera: Chalcidoidea: Agaonidae, Pteromalidae) Associated with Asian Fig Trees (Ficus, Moraceae) in Southern Africa: Asian Followers and African Colonists

ABSTRACT The Asian and Indo-Australasian fig tree species Ficus microcarpa and F. religiosa are widely-planted street and garden ornamentals in southern Africa and elsewhere. Like other fig trees, they depend for pollination on host specific fig wasps (Agaonidae). Their pollinators have also been widely introduced, and this allows the trees to become naturalised weeds. Both trees also support numerous non-pollinating fig wasps that can reduce seed or pollinator numbers, and a sub-set of these assemblages also now have wide distributions outside their native range. Two South African pollinators (Elisabethiella baijnathi, E. stuckenbergi), a galler (Otitesella uluzi) and a parasitoid (Sycoryctes species) occasionally succeed in reproducing in the figs of F. microcarpa, but in very small numbers. The tree's usual pollinator is absent but three Asian gallers of F. microcarpa are now widely established (Odontofroggatia corneri, Odontofroggatia galili and Walkerella microcarpae), and a fourth native species has expanded its host range and is developing as a parasitoid of the Odontofroggatia species (Sycophila punctum). In contrast, the Asian pollinator of F. religiosa (Platyscapa quadraticeps) has colonised South Africa and Zambia and is likely to be present throughout southern Africa. No non-pollinator associates have been recorded in the region. Without its usual pollinator, F. microcarpa cannot reproduce, but F. religiosa may eventually become established in areas with a suitable climate.


INTRODUCTION
Many fig trees (Ficus species, Moraceae) are easy to grow as roadside, hedgerow and garden trees, as well as making ideal bonsai specimens. As a result, they are common subjects in the horticultural trade and a number of species have been distributed by man around the world. There are 15 or more species of exotic fig trees present in Africa, of which at least eight are being commonly propagated (Burrows & Burrows 2003). Fig trees depend on host specific fig wasps (Agaonidae) for pollination, and consequently cannot reproduce sexually in the absence of their associated pollinator species (Janzen 1979;Wiebes 1979;McKey 1989;Weiblen 2002;Cook & Rasplus 2003;Herre et al. 2008;Cook & Segar 2010) (Compton 1993;Kerdelhué & Rasplus 1996;Kerdelhué et al. 2000;van Noort 2003;Cook & Segar 2010;Cruaud et al. 2011b;. These include ovule gallers and parasitoids, and they can reduce the reproductive success of both the trees and their pollinators (Weiblen 2002;Herre et al. 2008;Cook & Segar 2010).
Blastophaga psenes (L., 1758), the pollinator of the cultivated fig F. carica, was introduced to South Africa from California in 1908 for the caprification of non-parthe nocarpic fig varieties that otherwise would fail to produce edible fruits (Wohlfarter et al. 2011). Modern commercial cultivation of fresh figs for the consumer market usually focuses on artificially selected parthenocarpic cultivars that do not need pollination to produce ripe fruit, but there are still some caprifig orchards in South Africa that depend on the long-established populations of B. psenes for pollination (van Noort 2003;Wohlfarter et al. 2011).
Ficus microcarpa (sometimes known as the Malay Banyan, among numerous other common names), is also often referred to by its synonyms F. retusa and F. nitida. It is a common and widespread species, indigenous to the Asian and Indo-Australasian regions (Berg & Corner 2005;Tan et al. 2009). Within the native range of F. microcarpa, Chen et al. (1999) recorded 20 species of associated fig wasps in Taiwan, and there are additional species elsewhere within its natural range (Zhang & Xiao 2008;Feng & Huang 2010;Li et al. 2013;Wang & Compton, unpubl. data;J.-Y. Rasplus, pers. comm.). The tree is pollinated by Eupristina verticillata Waterston, 1921, a taxon that may represent a complex of closely-related species (Sun et al. 2011). Identification keys to the fig wasp species associated with F. microcarpa are available in publications by Chen et al. (1999) and Feng & Huang (2010).
Ficus microcarpa has been widely planted around the world as a garden, roadside and container tree (Condit 1969;Bouček 1988;Kobbi et al. 1996;Beardsley 1998;Yokoyama & Iwatsuki 1998;Chen et al. 1999;Burrows & Burrows 2003;Farache et al. 2009;van Noort & Rasplus 2010;Doğanlar 2012). In South Africa this fig tree species is cultivated in frost-free areas and is most prevalent in the coastal regions of the two Cape provinces, being particularly widespread in the Western Cape (Burrows & Burrows 2003). It is commonly planted as an ornamental roadside tree in Cape Town and Port Elizabeth and also in many of the smaller towns of the Western and Eastern Cape provinces. It is also grown as a container plant in malls and in city squares (Burrows & Burrows 2003).
Eupristina verticillata was deliberately introduced from the Philippines to pollinate F. microcarpa in Hawaii (Pemberton 1939), in order to promote propagation of the tree for a reforestation initiative (Beardsley 1998). However, natural seed dispersal by birds resulted in the rapid spread of F. microcarpa through the Hawaiian Islands (Williams 1939;van Zwaluwenburg 1940), where it has become a problematic weed (Beardsley 1998). Subsequently, E. verticillata spread without authorised introductions to most of the introduced range of F. microcarpa, including Australia (part), Bermuda, Brazil (São Paulo), Canary Islands, El Salvador, Hawaii, Honduras, Italy (Sicily), Japan (part), Madeira, Mexico, Puerto Rico, Solomon Islands, Tunisia, Turkey, United Arab Emirates, United States of America (California, Florida) (Lo Verde et al. 1991;Nadel et al., 1992;Kobbi et al. 1996;Yokoyama 1996;Beardsley 1998;Yokoyama & Iwatsuki 1998;Kopo nen & Askew 2002;van Noort & Rasplus 2010;Doğanlar 2012). The pre sence of the pollinator has resulted in seedlings developing in cracks and crevices of buildings, causing structural weaknesses, as well as to the tree becoming invasive in some natural areas (Ramirez & Montero 1988;McKey 1989;Lo Verde et al. 1991;Beardsley 1998).
Several of the NPFW species associated with F. microcarpa have also become established outside their native ranges, and two species are particularly widely distributed: Odontofroggatia galili Wiebes (Pteromalidae: Epichrysomallinae) and Walkerella mic rocarpae Bouček (Pteromalidae: Otitesellinae). Odontofroggatia galili is one of five described species in the genus that have been reared from figs of F. microcarpa and also the closely related F. prasinicarpa (Bouček 1988;Feng & Huang 2010). Odon tofroggatia species are gall-forming fig wasps that reproduce in the ovules of the host figs (Bouček 1988). Their galls are considerably larger than those formed by the pol linator. Odontofroggatia galili larvae can develop successfully in figs that have not been pollinated (Galil & Copland 1981). In urban environments this fig wasp is con sidered to be a nuisance, because gall development results in large, soft figs, which make a mess underneath the trees (Galil & Copland 1981). Over the last 40 years O. ga lili has expanded its range, probably aided by accidental transport by man inside figs. It arrived in Israel between 1970 and 1975 (presumably directly from Southeast Asia) and was subsequently reported from Florida, USA in 1986 (Galil & Copland 1981;Stange & Knight 1987). It had also reached the Greek island of Simi before September 1987, when the species was already numerous inside the figs of roadside trees (Compton 1989). Subsequently the species has also been reported from several other areas around the Mediterranean (Lo Verde & Porcelli 2010). A related species, Odontofroggatia ishii Wiebes, 1980 has been recently recorded from F. microcarpa in Turkey (Doğanlar 2012).
Walkerella microcarpae is a second ovule-gall forming species, with F. microcarpa as the only recorded host plant. It was originally described from the Americas, where it had colonised introduced F. microcarpa before the 1980s (Bouček 1993;Farache et al. 2009), and has been subsequently recorded from the Mediterranean area (Lo Verde et al. 2007;Doğanlar 2012). Within its native range its distribution extends from China to Papua New Guinea (Xu et al. 2005;Ma et al. 2013;Wang & Compton, unpubl. data;van Noort, unpubl. data).
Numerous species of fig wasps have been recorded from the figs of Ficus religiosa in its native range (Wiebes 1967), but only the pollinator, Platyscapa quadraticeps Mayr is recorded as having been introduced elsewhere. The presence of P. quadraticeps has been confirmed in countries around the Mediterranean (Galil & Copland 1981;van Noort & Rasplus 2010), and indirect evidence, based on the presence of F. religiosa seed lings, suggest that the pollinator is also present in Florida, Hawaii and Austra lia (Nadel et al. 1992;Bouček 1993;Randall 2007;Frohlich & Lau 2008). The pollina tor has also been reported from Zambia and South Africa (van Noort 2003), and Hyde et al. (2012) reported naturalised seedlings growing from a wall in Harare (Zimbabwe) in 2007, indicating that the pollinator is also likely to be present in Zimbabwe.
Introduced Specimens used for photography were point mounted on black, acid-free card for examination using a Leica M205C stereomicroscope with LED light sources. Images were acquired using the EntoVision multiple-focus imaging system. This system comprises a Leica M16 microscope with a JVC KY-75U 3-CCD digital video camera that fed image data to a notebook computer. The program Cartograph 5.6.0 was then used to merge an image series (representing typically 10-15 focal planes) into a single in-focus image. Lighting was achieved using techniques summarised in Buffington et al. (2005), Kerr et al. (2009) and Buffington & Gates (2009). All images presented in this paper are available through the Figweb resource (http://www.figweb.org).
The material is deposited in the following collections: SAMC -Iziko South African Museum, Cape Town; and SGCC -Stephen G. Compton collection, Rhodes University, South Africa and University of Leeds, UK.  (Bouček 1988;Chen et al. 1999;Feng & Huang 2010).

Family Eurytomidae Walker, 1832
Sycophila punctum Bouček, 1981 (Figs 8, 9) Material  region. They are excellent colonisers of islands , and some species can be dispersed by wind for tens or even hundreds of kilometres (Ahmed et al. 2009). Consequently, once they become established in a novel area, it is highly probable that they will spread across the entire population of their host fig tree in the region, however fragmented it may be. In South Africa, Ficus microcarpa (Fig. 7E) is planted as a garden ornamental or as a shade tree along streets or in parking areas in suburban situations and hence subpopulations may be separated by hundreds of kilometres. Two of the galler species associated with Ficus microcarpa, Walkerella microcar pae and Odontofroggatia galili were first recorded in 2007 in Cape Town and have now where the global horticultural stock was derived, i.e. they happened to be the species that became established in the source country that subsequently exported F. microcarpa figs globally, but it is also likely that features of their biology have facilitated their spread. Their ability to develop independently of the pollinator provides a clear advantage, and their adults may also be more physiologically resilient than some of the other species that have not spread beyond their native range.  crops than prior to the arrival of O. corneri, although this may reflect an increased proportion of the figs being colonised, rather than competitive exclusion. Odontofroggatia galili remains rare in the Cape Town samples. Clearly there is ongoing independent colonization occurring and it is likely that the pollinator will arrive in South Africa in the near future. In one of the Cape Town samples two pairs of O. galili females were preserved in copula with O. corneri males, together with pairs of both species in copula with their correct males in the same sample. These two species occur together in their native range, suggesting that this inter-species copulation is not a result of an artificial introduction effect and may result in hybrids if there is not a post-fertilization barrier in place.
In contrast to F. microcarpa, F. religiosa has its pollinator present in southern Afri ca and is reproducing successfully, although not spreading. According to Galil and Ei sikowitch (1968), F. religiosa is highly unlikely to establish in Israel, because of the con trast in conditions compared with the monsoonal climate of its natural distribution (Ga lil 1984). This is also likely to be true for much of southern Africa, but in higher rainfall areas F. religiosa may be able to colonise areas of natural vegetation. The pol linator has been established in Africa for at least 22 years and to date there is no in dication that the host fig is problematic by colonizing new areas.
The presence of adults of three species of African fig wasps in figs from one of the F. microcarpa crops sampled in Grahamstown and two different species in crops from Cape Town was unexpected. The three indigenous species recorded in Grahamstown in 2012 are all associated with the most common native fig tree in the area, F. burttdavyi and comprised the tree's pollinator (E. baijnathi), a putative parasitoid of the pollinator (Sycorctes sp. indesc. 'dark') and Otitesella uluzi, a species that is closely re lated to W. microcarpae and forms similar galls (Compton 1993). In 2013 two other indigenous African species both associated with F. burkei were recorded in Cape Town. The pollinator Elisabethiella stuckenbergi was represented by five females and a male in a crop from Grand West, clearly indicating that it was successfully reproducing. The other species, Sycophila punctum is a parasitoid, usually of indigenous epichrysomalline Lachaisea species (Compton & van Noort 1992), but in this crop of F. microcarpa would have probably been parasitizing either of the two introduced epichrysomallines, O. corneri or O. galili, and hence is able to use hosts from different genera. All these local species were present in tiny numbers, but these records nonetheless show that fig wasps can be capable of successfully galling and completing their development in a Ficus species that is only distantly-related to their normal host (F. burtt-davyi and F. burkei are placed in Ficus subgenus Urostigma, section Galoglychia, whereas F. microcarpa is placed in subgenus Urostigma, section Urostigma).