Solanum mauritianum Scopoli and Solanum sisymbriifolium Lamarck are major exotic weeds in South Africa, while Solanum viarum Dunal is similarly problematic in the United States of America. All three species are native to northeastern Argentina and southeastern Paraguay, where they were surveyed for natural enemies in February 1998. Insect agents for Solanum weeds have a tendency to extend their host ranges to include non-target Solanum species, in particular cultivated eggplant (S. melongena L.), during laboratory trials, making it difficult to promote their release. To facilitate the interpretation of such results, other native and cultivated Solanum species that grew in close proximity to the target species were also surveyed to give an indication of the insects’ field host ranges. During the survey period, 19 insect herbivore species were recorded on S. mauritianum, while 8 species were recorded on each of S. sisymbriifolium and S. viarum. Based on the insects’ occurrence, abundance and damage to their target weeds, and their absence on other non-target Solanum species, several natural enemies that warrant further investigation were identified. These include 5 species associated with S. mauritianum and 2 species associated with each of S. sisymbriifolium and S. viarum. With rare exceptions, these insects were normally associated with a single host species and none attacked cultivated eggplant.
South American species of Solanum L. (Solanaceae) include weeds of agricultural and environmental importance in South Africa and the United States of America. Two species, Solanum mauritianum Scopoli (bugweed, woolly nightshade) and Solanum sisymbriifolium Lamarck (wild tomato, sticky nightshade), were targeted for biological control in South Africa (Olckers 1999, Olckers et al. 1999), while a third, Solanum viarum Dunal (tropical soda apple), was targeted in the USA (Medal et al. 1996, Medal et al. 1999). All three species are native to northeastern Argentina, southern Brazil, Paraguay and Uruguay. During February 1998, a trip to northeastern Argentina and southeastern Paraguay was undertaken by scientists from Argentina, South Africa and the USA for the purpose of recording and collecting promising natural enemies of S. mauritianum, S. sisymbriifolium and S. viarum.
Biological control programmes against Solanum weeds have been complicated by introduced insect agents feeding on non-target congeneric species during quarantine evaluations (Olckers 1999, Olckers et al. 1999). Although these agents feed exclusively on Solanum species and are unable to utilize other solanaceous genera, cultivated eggplant (S. melongena L.) and certain native Solanum species are particularly susceptible to feeding by these agents, ensuring difficulties in promoting their release. These concerns are aggravated by revelations that in the USA, nearly all native plants that have become hosts for biocontrol agents belong to the same genus as the target weed (Pemberton 2000). In an attempt to collect information on the field host ranges of candidate agents for S. mauritianum, S. sisymbriifolium and S. viarum, all native Solanum species encountered during the trip were surveyed for insect herbivores. Efforts were also made to locate and examine eggplant cultivations growing in close proximity to natural populations of all three target weed species.
In this paper, we report on the insect herbivores associated with native Solanum species and cultivated eggplant in northeastern Argentina and southeastern Paraguay. Comments on the suitability of potential biological control agents for S. mauritianum, S. sisymbriifolium and S. viarum are made in the light of these observations.
Materials and Methods
Field observations and collections of insects associated with S. mauritianum, S. sisymbriifolium and S. viarum were made during a 7-day survey of native Solanum species and cultivated eggplant, encountered at several sites in northeastern Argentina and southeastern Paraguay, from 15-21 February 1998. Some 23 localities and 8 plant species were surveyed (Table 1).
At each locality, natural stands of plants were scanned for ectophagous herbivores and damaged stems, flowers and fruit were dissected to observe endophagous species. Since no specific sampling protocol was followed, collecting times varied at each locality, with more time spent at sites where the plant populations supported rich insect faunas. The phenological stages of the 8 Solanum species surveyed at the 23 sites were very similar in that, with few exceptions, the populations were flowering.
Insect species that were deemed to be ‘common’ were present at 20% or more of the localities where a particular Solanum species was surveyed. By contrast, ‘abundant’ species were those that were found in high numbers when encountered, but were not necessarily common. Voucher specimens of plants and insects are lodged in the collections of the South American Biological Control Laboratory (United States Department of Agriculture, Buenos Aires, Argentina) and the Cedara Weeds Laboratory (Plant Protection Research Institute, Hilton, South Africa).
Insects Associated with Solanum mauritianum
Nineteen insect herbivore species were associated with S. mauritianum (Table 2) at the 14 sites where this species was surveyed (Table 1). Of these, at least 10 species were previously collected on this plant (Neser et al. 1990). While 11 of the 19 species were also recorded on other Solanum species, 8 were recorded on S. mauritianum only (Table 2, Table 3). Eight herbivore species were considered to be common, of which 6 species were abundant at the sites.
On the basis of their incidence, abundance, resultant damage and observed host ranges, 5 of these herbivore species are considered to have potential as biocontrol agents (Table 3). These include the leaf-mining flea beetle Acallepitrix sp. nov. (Chrysomelidae), stem-boring weevils Collabismus notulatus Boheman and Conotrachelus prob. squalidus Boheman (both Curculionidae) and flower-feeding weevils Anthonomus morticinus Clark and A. santacruzi Hustache (Curculionidae). The former two species are uncommon and occur in low numbers, while the latter three species are common and mostly occur in high numbers when encountered (Table 3). The two Anthonomus species are morphologically very similar and were collected together at one locality. Despite the recovery of A. santacruzi on Solanum fastigiatum Willd. at one site, the high levels of floral damage inflicted has necessitated that this species warrants further investigation. All 5 candidate agents were imported into quarantine in South Africa at the conclusion of this trip (Olckers 1999).
Other species that were common, abundant, or both, but were not considered as potential biocontrol agents include the stem-boring beetle Nealcidion bicristatum (Bates) (Cerambycidae), an unidentified species of Membracidae, a species of Nezara (Pentatomidae), the lace bug Corythaica cyathicollis (Costa) (Tingidae), the leaf-mining moth Acrolepia xylophragma (Meyrick) (Acrolepiidae) and the flower-feeding beetles, Nycterodina sp. (Chrysomelidae)and Carpophilus sp. (Nitidulidae) (Table 3). Reasons for this include broad field host ranges (e.g. C. cyathicollis), reported pest status (e.g. N. bicristatum), broad host ranges in quarantine (e.g. A. xylophragma) and insufficient information on the damage inflicted (e.g. Membracidae, Carpophilus sp.) (Olckers 1999).
A notable exception from the herbivore fauna was the leaf-sucking lace bug Gargaphia decoris Drake (Tingidae) which was released in South Africa against S. mauritianum (Olckers 1999, Olckers 2000). This insect was imported following a single collection made near the Iguazu Falls (MS) in 1995, but was not observed in the same area during this trip and may thus be a rare species.
Insects Associated with Solanum sisymbriifolium
Eight insect herbivore species were recorded on S. sisymbriifolium (Table 2) at the 8 sites where this species was surveyed (Table 1). Four of these species are polyphagous (e.g. Diabrotica speciosa Germar) while the sap-sucking Amblyophallus maculatus Funkhonser (Membracidae) was associated with several other Solanum species (Table 3). Of the remaining 3 species, the unidentified species of Miridae was only recorded on S. sisymbriifolium, while the leaf-feeding tortoise beetle Gratiana spadicea (Klug) and flower-feeding weevil Anthonomus sisymbrii Hustache were also recorded on S. viarum, at one site where this species grew in close proximity to S. sisymbriifolium.
Five herbivore species were common and two of these were abundant at the sites (Table 3). Gratiana spadicea was the most common, abundant and damaging herbivore and was recovered at all 8 sites. The only species of importance from a biocontrol perspective were G. spadicea and A. sisymbrii, since there is insufficient information on the damage caused by the Miridae. Because these surveys were focused primarily on S. mauritianum and S. viarum, none of these insect species were imported into quarantine in South Africa at the conclusion of this trip.
Insects Associated with Solanum viarum
Eight insect herbivore species were associated with S. viarum (Table 2) at the 12 sites where this plant was surveyed (Table 1), of which 6 species were previously collected on this plant (Medal et al. 1996). While 6 herbivore species were recorded on other species of Solanum, 2 species were collected on S. viarum only (Table 2). Of the latter species, the leaf-feeding tortoise beetle Metriona elatior Klug (Chrysomelidae) appears to be host specific while the fruit-boring moth Neoleucinodes elegantalis Guenee (Pyralidae) is reported to attack tomato crops (Medal et al. 1996). Another tortoise beetle, Gratiana boliviana Spaeth, may also be suitably host specific, despite the collection of a single specimen on Solanum palinacanthum Dunal at one site where this species grew in close proximity to S. viarum.
Four herbivore species were common during this trip, namely G. boliviana, M. elatior, A. maculatus and the defoliating butterfly Mechanitis lysimnia Fabricius (Nymphalidae) (Table 3). All except M. elatior were abundant when encountered. A few specimens of G. spadicea and A. sisymbrii, which are normally associated with S. sisymbriifolium, were collected on S. viarum on one occasion (see above). At this site some flowerbuds of S. viarum contained larvae of A. sisymbrii, suggesting that this plant may be an alternative host for the weevil. The congeneric Anthonomus cf. tenebrosus Boheman which was previously collected on S. viarum (D. E. G., unpublished data), was not recovered on the plants during this survey. However, 3 specimens identified as A. tenebrosus were collected on an unidentified species of Solanum (see below).
On the basis of their incidence, abundance, damage levels and observed host ranges, only G. boliviana and M. elatior are important from a biocontrol perspective. Both species were collected for further studies in the laboratory in Argentina and the USA.
Insects Associated with Other Solanum Species
The most common of the remaining Solanum species was S. fastigiatum which was surveyed at 5 sites (Table 1). Of the 12 insect herbivore species observed on this plant (Table 2), most were also collected on other Solanum species. Species that were only recorded on S. fastigiatum included a tortoise beetle (probably a species of Gratiana), the leaf beetle Platyphora quadrisignata (Germar) (both Chrysomelidae) as well as an unidentified weevil (Curculionidae) and moth (Gelechiidae), both of which fed on the flowers. The most notable observation was the recovery of several specimens of A. santacruzi on flowers of S. fastigiatum at one site in Paraguay. This species is normally associated with S. mauritianum, but has also been recorded on Solanum granuloso-leprosum Dunal (Clark & Burke 1996), a species very closely related to and often confused with S. mauritianum (Kissmann & Groth 1997).
Three other Solanum species, S. atropurpureum (Schrank), S. palinacanthum and an unidentified species, were surveyed at only one or two sites (Table 1). The only noteworthy insects recorded on these (Table 2) were a single specimen of G. boliviana on the foliage of S. palinacanthum and 3 specimens of A. tenebrosus on the flowers of the unidentified Solanum.
Insects Associated with Eggplant Cultivations
Eggplant is not cultivated extensively in the areas surveyed and only 2 cultivations, that were untreated with pesticides and in close proximity to S. mauritianum (2 sites), S. sisymbriifolium (2 sites) or S. viarum (1 site), were located (Table 1). Eleven insect herbivore species were recorded on the crop (Table 2), although most of these occurred at low, undamaging levels. Species that caused the most damage were the lace bug C. cyathicollis and leaf-feeding flea beetle Epitrix prob. parvula (F.), both of which are recorded as pests of eggplant (Silva et al. 1968). In addition, the membracid A. maculatus and defoliating butterfly M. lysimnia, which were previously reported to cause significant damage to S. viarum (Medal et al. 1996), were also observed to attack the crop.
The most important observations on eggplant were the absence of several insects with biocontrol potential, despite their presence on natural host plants that were in close proximity (within 20 m) to the cultivations. These species include A. santacruzi, A. morticinus, C. prob. squalidus, C. notulatus (all on S. mauritianum), G. spadicea (on S. sisymbriifolium) and G. boliviana (on S. viarum).
The surveys confirmed the unsuitability of some of the insect species that were previously introduced into quarantine for screening as biocontrol agents. Corythaica cyathicollis and N. bicristatum were the first candidate agents imported for S. mauritianum in South Africa, but were rejected before tests were initiated because of published host records implicating several families of plants (Silva et al. 1968, Olckers 1999). The broad host range and pest status of C. cyathicollis was confirmed by these surveys and by preliminary trials in the USA, where it was evaluated as an agent for S. viarum (J. C. M., unpublished data). Although N. bicristatum was only collected on S. mauritianum during these surveys, adults have been reared from larvae collected in the stems of Sambucus australis Cham. & Schlecht. (Caprifoliaceae) in Buenos Aires Province (Di Iorio et al. 1998) which, being outside the range of S. mauritianum in Argentina, confirms that this species is polyphagous. The broad host range of A. maculatus, another candidate agent for S. viarum, during laboratory trials in the USA (J. C. M., unpublished data), was confirmed by its recovery on several non-target Solanum species including cultivated eggplant. None of the above mentioned species will thus be considered for release in South Africa or the USA.
Despite the findings that 58% and 75% of the S. mauritianum and S. viarum faunas, respectively, were also collected on other species of Solanum, the surveys suggested that at least 5 candidate agents for S. mauritianum and 2 for S. viarum warrant further investigation. Of the potential agents for S. mauritianum, the flower-feeding weevil A. santacruzi and leaf-mining flea beetle Acallepitrix sp. nov. are currently undergoing host-specificity tests in South Africa (Olckers 1999), while the second flowerbud weevil, A. morticinus, is under evaluation in Brazil. Similar evaluations on the leaf-feeding tortoise beetles M. elatior (Medal et al. 1999) and G. boliviana (Medal et al. 2001) in Argentina, Brazil and the USA have been concluded. Permission for the release of both M. elatior and G. boliviana in the USA has been sought, but has been delayed pending further investigation. By contrast, permission to release A. santacruzi and Acallepitrix sp. nov. in South Africa has not yet been sought because of feeding on non-target Solanum species in quarantine (T. O., unpublished data), necessitating that further work in South America be carried out to elucidate the agents’ field host ranges.
Although the surveys were largely focused on S. mauritianum and S. viarum, observations on S. sisymbriifolium confirmed the importance of two natural enemies. The leaf-feeding tortoise beetle G. spadicea was the most common, abundant and destructive species, while the flower-feeding weevil A. sisymbrii was less common and abundant but is potentially very damaging because of its ability to reduce fruit set. Gratiana spadicea was released in South Africa for the biocontrol of S. sisymbriifolium, despite feeding on eggplant and 8 native South African Solanum species during quarantine evaluations (Olckers et al. 1999). Collections of the beetle on only two host plants during this survey and the absence of attacks on eggplant, provide some support for the decision to release this agent. Anthonomus sisymbrii has also been considered for introduction into South Africa (Olckers et al. 1999) and these surveys support this conclusion.
We thank M. P. Hill (Plant Protection Research Institute) and three anonymous referees for comments on the manuscript. The staff of the South American Biological Control Laboratory (United States Department of Agriculture, Agricultural Research Service, Buenos Aires) are thanked for hosting two of the authors (T. O. and J. C. M.) during their stay in Argentina. Information on eggplant cultivation in Misiones was supplied by staff of the Instituto Nacional de Tecnología Agropecuaria (Posadas, Misiones). The identities of N. bicristatum, the different species of Anthonomus and G. boliviana were confirmed by O. Di Iorio (SABCL), W. E. Clark (Auburn University, Auburn, USA) and Z. J. Buzzi (Universidade Federal do Paraná, Curitiba, Brazil) respectively. Financial support for this survey was provided by the ‘Working for Water’ Programme (Department of Water Affairs and Forestry, South Africa), the USDA-ARS, the Animal and Plant Health Inspection Service (USDA) and the Interstate Pest Control Fund through the Florida Department of Agriculture and Consumer Services (Division of Plant Industry).
Table 1. Localities in Argentina and Paraguay where different species of Solanum were surveyed for insect herbivores.
Insect herbivores associated with species of Solanum in Argentina and Paraguay.
Table 3. Incidence, abundance and field host range of insect herbivores associated with Solanum mauritianum, Solanum sisymbriifolium and Solanum viarum in Argentina and Paraguay. (* = species that have potential as biocontrol agents)