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Importance of preintroduction surveys in the biological control of Solanum weeds in South Africa
Agriculture Ecosystems & Enwronment ELSEVIER
Agriculture, Ecosystemsand Environment 52 ( 1995 ) 179-185
Importance of preintroduction surveys in the biological control of Solanum weeds in South Africa T. Olckers a'*, P.E. Hulley b aPlantProtectionResearch Institute, Private Bag X9059, Pietermaritzburg3200, South Africa bDepartment of Zoology and Entomology, Rhodes University, Grahamstown 6140, South Africa Accepted 31 May 1994
Abstract
Three exotic Solanum weeds, Solanum elaeagnifolium Cav., Solanum mauritianum Scop. and Solanum sisymbriifolium Lam. (Solanaceae), are targets for biological control in South Africa. Preintroduction surveys of the insect herbivores attacking these, as well as native and cultivated species of Solanum, have proved useful in several ways. Although there is a diverse, mainly oligophagous, herbivore fauna on native Solanum spp., that of the exotic weeds is mainly polyphagous and low in diversity and numbers. Feeding niches on introduced weeds are either vacant or underutilized, ensuring a wide scope for the selection of exotic biocontrol agents. Similarities between potential agents and native Solanum herbivores suggest that the former may recruit native parasitoids, a fact that has to be considered in the selection process. The surveys also helped to resolve a conflict of interest, caused by most candidate agents accepting the introduced crop plant Solanum melongena L. (eggplant) in specificity tests. Although a number of native Solanum oligophages attacked neglected eggplant fields, damage to crops is precluded by the pesticide regimes aimed at several generalist pests. Imported agents are no more a risk than native Solanum feeders, which are not regarded as pests. The surveys support the view that exotic agents should be introduced to control Solanum weeds.
Keywords: Biologicalcontrol; Solanaceae;South Africa
1. Introduction The exotic Solanum elaeagnifolium Cav. (silverleaf nightshade) and Solanum mauritianum Scop. (bugweed) are major weeds in South Africa, with the minor weed Solanum sisymbriifolium Lam. (wild tomato) becoming increasingly important. S. elaeagnifolium is native to the southwestern USA, Mexico and South America, and S. mauritianum and S. sisymbriifolium orig* Corresponding author.
inate from South America (Symon, 1981 ). South Africa has about 50 native and two cultivated Solanum spp. (Gibbs Russell et al., 1987). Of the latter, Solanum tuberosum L. (potato) is cultivated extensively in South Africa and Solanum melongena L. (eggplant, brinjal) is a crop of lesser importance (Annecke and Moran, 1982). The importance of biological control in the management of exotic Solanum weeds was reviewed by Olckers and Zimmermann ( 1991 ). Preintroduction surveys of the herbivores of exotic, native and cultivated Solanum spp. were
0167-8809/95/$09.50 © 1995 Elsevier Science B.V. All rights reserved SSDI 0167-88090 ( 94 ) 00537-0
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undertaken in South Africa to determine: ( 1) the diversity of herbivore species on native Solanum spp. and the extent to which these may be preadapted to exotic species, (2) the biology, host range and relationships of the native herbivores, which could influence their feeding on exotic Solanum spp., (3) the numbers and impact of native herbivores attacking introduced weedy and cultivated species, (4) whether any potential biocontrol agents had already entered the country accidentally, as occurred for Trichapion lativentre (Brguin-Billecocq), a successful control agent ofSesbania punicea (Cav.) Benth. (Hoffmann and Moran, 1991 ), and (5) the taxonomic and ecological similarities between native herbivores and exotic agents to determine the extent to which native parasitoids may transfer to imported hosts.
2.2. Impact of native parasitoids on imported agents A field colony of an undescribed species of Frumenta (Gelechiidae), on an experimental plot of S. elaeagnifolium at the Uitenhage Weed Laboratory ( 33 ° 43'S; 25 ° 26'E), permitted observations on the impact of native parasitoids on imported American agents. These observations provided evidence to support predictions based on the results of the surveys. The plot comprised a 2 m × 2 m stand of plants on which 570 neonate caterpillars were placed on flowerbuds and budless shoots, where they formed seedless fruit and stem galls respectively. The neonates were released between November 1989 and January 1990 and survival was monitored by counts of galls and emerged moths. The galls were removed and dissected at the end of May 1990, when the plants senesced.
2. Methods 3. Herbivores on native Solanum spp.
2.1. Faunistic surveys Insect herbivores were collected on all exotic, native and cultivated Solanum spp. encountered in the eastern Cape Province, Transvaal and Natal regions of South Africa, between 1985 and 1992. During each collection, 10-20 plants were scanned for ectophagous herbivores in the field and representative samples were taken for further examination. Stems were dissected for borers and the foliage was scrutinized for 'cryptic' ectophages and other endophages. Fruit and flowers were also collected, one half being frozen for subsequent dissection and the remainder kept in emergence cages to allow for any immature herbivores or parasitoids to complete development. Immature stages of ectophagous herbivores were also kept in emergence cages for the same reason. Only insects feeding or reproducing on the plants were recorded. Voucher specimens of insect herbivores and parasitoids were placed in the Albany Museum (Grahamstown) and in the National Collection of Insects (Pretoria). The results of each regional survey were presented by Olckers and Hulley ( 1989, 1991a, 1994) and Hill et al. (1993).
Native Solanum spp. were attacked by a diverse insect herbivore fauna (Olckers and HulTable 1 Diversity of insect herbivores on exotic, cultivated and native species of Solanum in South Africa
Solanum species
Number of herbivore species a Spec.
Genr.
Total
Rank b
12 5
9 17
21 22
6 8
2
10
12
9
17
11
28
3
27 22 16 15
28 15 17 5
55 37 38 20
1 2 4 5
8
7
15
7
Exotic
S. elaeagnifolium S. mauritianum S. sisymbriifolium Cultivated
S. melongena Native
S. panduriforme S. incanum S. linnaeanum S. coccineum S. rigescens
a Specialists (Spec.) are insects specific to the genus Solanum; generalists (Genr.) attack plant families other than Solanaceae. b According to diversity of specialist herbivore species.
T. Olckers, P.E. Hulley / Agriculture, Ecosystems and Environment 52 (1995) 179-185
181
C h e w e r s ~ (37)
Suckers ~25)
Fruit-feeders
~
/
/
n-
ii!ill
\
\
~.
"~..'~ Flower-feeders ,3) "~'.. "..~/ L e a f - miners t2) \~.v^ ~ / ~all- formers
5
14)
4 NATIVE PLANTS
i!ilii i:?i: :i:i:! !:?i: iiili! i!iiii iiiiil
~i!iiii iiiiii
~iiiiiiilili!
ili~i "
?!:!: :i:i:i i!iiii
~i!i!ii ~i:!:i ii!~i~ :i:!:i ?i:? iiiii!
iiii!i +:<
~ii:/ii] iiiii~
o i!iili :i:!:i
Chewers
/ : ~ \ Fruit(5~eeders
,1,, /
2 E
\
~
Flowe~-feeders
-=1
(18)
I
2 EXOTIC PLANTS
I
,
4
5
Number
I
6
l
7
l
8
9
H 10
of host plants
Fig. 2. Number of host plant species recorded for common insect herbivores associated with native Solanum spp. in South Africa.
Ch~,ers
,1,,
3
iilii! :i:!:! iiiiii :i:!:i !:i:i: i!iiii
\ 12>
CULTIVATED PLANTS
Fig. I. Insect herbivores associated with native, exotic and cultivated Solanum spp. in South Africa. Endophagous guilds are indicated by shaded sectors; numbers of insect species per group are indicated in parentheses. Plant categories as in Table 1.
ley, 1989, 1991a; Table 1), comprising many species that occurred over a wide geographic range and appeared to be specific to the genus Solanum. These specialist species constituted potential colonists, from which potentially preadapted species might attack introduced Solanum spp. In addition, a number of generalists, some of which were consistently associated with the genus, contributed to the often high levels of damage. The guild structure of the herbivore "pool' (Fig. 1 ) showed a predominance of chewing and sucking ectophagous species. The endophagous species (27% of the community) included stemborers, gall-formers, leaf-miners, fruit-feeders and flower-feeders. Native Solanum herbivores thus have representatives in all major guilds. Of the specialist herbivores (i.e. those specific
to the genus), 75% occurred on at least three host Solanum spp. (Fig. 2 ), indicative of oligophagy. This, and the number of generalist species (2558% of native Solanum herbivores; Table l ), made preadaptation to feeding on exotic Solanum spp. very likely.
4. Role of native insects in Solanum biocontrol
Exotic plants may be damaged by herbivores of native plants when these include close relatives (e.g. exotic thistles (Asteraceae) in the USA (Goeden, 1971, 1974; Goeden and Ricker, 1986 ) ). However, the three exotic Solanum spp. had few, largely generalist, herbivores (Table 1 ) and were relatively undamaged in comparison to native plants (Olckers and Hulley, 1989, 1991 a; Hill et al., 1993). No trace was found of any accidentally introduced herbivores. Twelve specialist species were recorded on S. elaeagnifolium, five on S. mauritianum and two on S. sisymbriifolium (Table 1 ), but in low numbers and causing only minor damage. Exotic species differed from native plants (Fig. 1 ) in having no gall-formers or leaf-miners. Endophages comprised 18% of the community, although 71% were
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72. OIckers, P.E. Hulley / Agriculture, Ecosystems and Environment 52 (1995) 179-185
Table 2 Similarities between candidate agents for S. elaeagnifolium and native Solanum insectsa Candidate agent
Native insectsb
Parasitoids c
Gratiana spp. (D) (Chrysomelidae: Cassidinae )
Conchyloctenia spp. (D) (Chrysomelidae: Cassidinae)
1 sp. (egg) 2 spp. (pupal)
Leptinotarsa spp. (D) (Chrysomelidae: Chrysomelinae )
Conchyloctenia spp. (D) (Chrysomelidae: Cassidinae ) Epilachna spp. (D) (Coccinellidae)
Asabove
Frumenta nephelomicta ( FG ) (Gelechiidae)
Scrobipalpa concreta ( FG ) (Gelechiidae)
4 spp. (larval)
Frumenta sp. (FG/SG) (Gelechiidae)
Scrobipalpa concreta ( FG ) Unidentified sp. (SG) Scrobipalpa incola ( SG ) (All Gelechiidae )
As above 4 spp. (larval) 2 spp. (larval)
Trichobaris texana ( SB ) (Curculionidae)
Oberea trigonalis (SB) (Cerambycidae) Pseudagrilus sp. (SB) (Buprestidae)
Unknown
Carpophilus sp. (FL) (Nitidulidae)
Pria sp. (FL) (Nitidulidae)
Unknown
Symmetrischema ardeola (FL ) (Gelechiidae)
Scrobipalpa concreta ( FG ) (Getechiidae)
4 spp. (larval)
Unidentified sp. (SG) (Cecidomyiidae)
Unidentified sp. (LG) (Cecidomyiidae)
10 spp. (larval)
Anthonomus sp. (FL) (Curculionidae)
Pria sp. (FL) (Nitidulidae)
Unknown
Gargaphia arizonica (D ) (Tingidae)
Urentius hystricellus (D) (Tingidae)
Unknown
Zonosemata vittigera ( FR ) (Tephritidae)
Silba ophyroides (FR ) (Lonchaeidae) Atherigona orientalis (FR ) (Muscidae)
Unknown
2spp.(pupal)
Unknown
Unknown
a D, defoliators; SB, stem-borers; SG, stem-gallers; FL, flower-feeders; FG, flower-gallers; FR, fruit-feeders; LG, leaf-gallers. b Either close relative and/or with similar biology. c Parasitoids of native Solanum insects are indicated. polyphagous fruit-feeders and thus not part o f the regular S o l a n u m h e r b i v o r e 'pool'. In S. e l a e a g n i f o l i u m 57%, in S. m a u r i t i a n u m 23% a n d in S. s i s y m b r i i f o l i u m 17% o f the herbivores originated f r o m the native S o l a n u m herbivore 'pool', the rest being generalist species
(Table 1 ). This reflects the fact that S. elaeagnif o l i u m belongs to the s a m e subgenus as the native species a n d has close relatives a m o n g s t the native plants, whereas S. m a u r i t i a n u m belongs to a subgenus o f S o l a n u m which is not represented in Africa ( D ' A r c y , 1972; Jaeger a n d H e p -
T. Olckers, P.E. Hulley / Agriculture, Ecosystems and Environment 52 (1995) 179-185
per, 1986). S. sisymbriifolium, however, belongs to the same subgenus as native species but is much more heavily endowed with glandular trichomes, which rarely occur on native species (Hill et al., 1993). The exotic Solanum spp. are underexploited so far as their defences are probably unique, and herbivores of native Solanum spp. are not preadapted to overcome them. The only insects inflicting appreciable damage were polyphagous hemipterans which caused sporadic seed mortality of 46-67% on S. elaeagnifolium (Olckers and Hulley, 1991b). Native insects are unlikely to contribute much to the control of the three weeds, leaving wide scope for selecting exotic biological control agents.
5. Impact of native parasitoids on imported agents Native predators and parasitoids often interfere with agents imported for weed control, often preventing establishment. According to Goeden and Louda (1976), predators involved were mainly polyphagous, with parasitoids often transferring from closely related native herbivores. The preintroduction surveys showed that South African Solanum faunas included many herbivores with taxonomic and ecological similarities to potential agents from the Americas, which increased the chances for parasitoids to attack them. This was particularly true of agents for S. elaeagnifolium (cf. Table 2 and Zimmermann, 1974; Neser, 1984; Wapshere, 1988). The surveys provided the opportunity to rear and identify parasitoids and there is evidence to predict that many candidate agents for S. elaeagnifolium would rapidly be parasitized in South Africa. Laboratory studies on American tortoise beetles (Gratiana spp.) indicated that pupae were susceptible to eulophid parasitoids of tortoise beetles (Conchyloctenia spp.) associated with native Solanum spp. (Siebert, 1975 ). Field observations on the American fruit- and stemgalling gelechiid (Frumenta sp.) revealed that moths emerged from only 14% of the galls initially formed. Although mortality was also caused
183
by desiccation of early instars and moths failing to emerge properly, 51% of mortality could be attributed to parasitism. The parasitoids were not identified because galls were dissected after they had emerged. However, they were most likely parasitoids of three gelechiid moths which form galls on at least six native Solanum spp. (Table 2; Olckers and Hulley, 1991 c). On the other hand, defoliating Leptinotarsa spp. (Chrysomelinae), whose closest native relatives are Conchyloctenia spp. (Cassidinae), are less likely to attract native parasitoids. Leptinotarsa larvae are unique in that they pupate underground and are also larger, more active and quicker in development than Conchyloctenia spp., in which parasitism is concentrated on the egg stage. Eggs of Leptinotarsa spp. may be vulnerable, but are morphologically similar to those of native Epilachna spp. (Coccinellidae) from which no parasitoids were reared. Leptinotarsa spp. are therefore considered the most promising biocontrol candidates for S. elaeagnifolium (Olckers and Zimmermann, 1991 ). Other agents, like Trichobaris texana LeConte and Anthonomus sp., which have no close relatives among herbivores of native Solanum spp. (Table 2), may thus also be suited for release on S.
elaeagnifolium. 6. Suitability of agents for release According to Annecke and Moran (1982), pests of introduced solanaceous crops such as potatoes ( S. tubersum ), tomatoes ( Lycopersicon spp.), peppers (Capsicum spp.), eggplant (S. melongena ) and tobacco (Nicotiana tabacum L. ) are mostly polyphagous species. Recruitment of native Solanum herbivores thus appears negligible in South Africa, as for exotic Solanum weeds. However, the present surveys indicate a far greater diversity of insects injurious to eggplant than reported in the literature (Olckers and Hulley, 1994). Field crops were attacked by 28 insect species, 61% of which were specialists from the Solanum herbivore 'pool' (Table 1 ). Some of them caused considerable damage in the absence of the usual pesticide regimes. The ease
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T. Olckers, P.E. Hulley / Agriculture, Ecosystems and Environment 52 (1995) 179-185
with which native herbivores feed on eggplant was exemplified by a leaf-galling cecidomyiid, previously recorded on one native Solanum species only (Olckers and Hulley, 1991 c ). Virtually all groups of herbivores associated with native Solanum spp. were represented on eggplant (Fig. 1 ) and endophages comprised 29% of the community. These results reflect the fact that eggplant is very closely related to some native Solanum spp. (D'Arcy, 1972; Pearce and Lester, 1979). Eggplant may lack chemical defences, because of selection for palatability, or else may have defences very similar to that of native species which native herbivores have already overcome. These findings also imply that imported agents could transfer to poorly defended Solanum crops like eggplant. Indeed, this occurred during specificity tests with four promising species of Gratiana and Leptinotarsa (Chrysomelidae); although solanaceous crops like potatoes, tomatoes, peppers and tobacco were unacceptable to them, they all fed and survived on eggplant (Neser et al., 1990; Olckers and Zimmermann, 1991 ); yet none of these candidates are known to attack eggplant on the American continent (Neser et al., 1990; Olckers and Zimmermann, 1991 ). However, the readiness with which many of the native Solanum herbivores attacked eggplant suggests that imported agents could do so during stress situations, as they did in the laboratory. Biocontrol of Solanum weeds in South Africa had thus reached a stalemate in that releases of agents were perceived as risky. The preintroduction surveys revealed that eggplant cultivations are protected from generalists (e.g. spider mites, lepidopterous larvae, aphids ) by a range of broad-based pesticides (e.g. monocrotophos, deltamethrin, endosulphan). Although highly toxic chemicals (e.g. monocrotophos, profenofos) were applied as required, most pesticides were, on average, applied once every 2 weeks. It was clear that these severe pesticide regimes also completely protected eggplant from native Solanum oligophages, to the extent that they are not regarded as pests (cf. Annecke and Moran, 1982; Olckers and Hulley, 1994). Furthermore, chemical trials (Olckers and Hulley, 1994) indicated that the more common pes-
ticides were lethal to Leptinotarsa spp. and should thus prevent any agents that might move onto eggplant from persisting. These lines of evidence suggest that imported agents are no more a threat than native insects. We therefore argue that imported insects could be released to control Solanum weeds, in spite of the apparent presence of a crop at risk.
Acknowledgements The authors thank G.B. Dennill, R.L. Kluge and anonymous referees for comments on the manuscript. The senior author is grateful to The Anglo American and De Beers Chairman's Fund for a travel grant which enabled him to present this work at the VIII International Symposium on Biological Control of Weeds, held at Lincoln University, New Zealand.
References Annecke, D.P. and Moran, V.C., 1982. Insects and Mites of Cultivated Plants in South Africa. Butterworths, Durban. D'Arcy, W.G., 1972. Solanaceae studies 2: Typification of subdivisions of Solanum. Ann. Mo. Bot. Gard., 59: 262278. Gibbs Russell, G.E., Welman, W.G., Retief, E., Immelman, K.L., Germishuizen, G., Pienaar, B.J., van Wyk, M., Nicholas, A., de Wet, C., Mogford, J.C. and Mulvenna, J., 1987. List of Species of Southern African Plants, Edition 2, Part 2. Mem. Bot. Surv. S. Afr. No. 56. Botanical Research Institute, Department of Agriculture and Water Supply, South Africa. Goeden, R.D., 1971. The phytophagous insect fauna of milk thistle in Southern California. J. Econ. Entomol., 64: 1101-1104. Goeden, R.D., 1974. Comparative surveys of the phytophagous insect faunas of Italian thistle, Carduus pycnocephalus, in Southern California and Southern Europe relative to biological weed control. Environ. Entomol., 3: 464-474. Goeden, R.D. and Louda, S.M., 1976. Biotic interference with insects imported for weed control. Annu. Rev. Entomol., 21: 325-342. Goeden, R.D. and Ricker, D.W., 1986. Phytophagous insect faunas of two introduced Cirsium thistles, C. ochrocentrum and C. vulgare, in Southern California. Ann. Entomol. Soc. Am., 79: 945-952. Hill, M., Hulley, P.E. and Olckers, T., 1993. Insect herbivores on the exotic weeds Solanum elaeagnifolium Ca-
T. Olckers, P.E. Hulley / Agriculture, Ecosystems and Environment 52 (1995) 179-I85 vanilles and S. sisymbriifolium Lamarck (Solanaceae) in South Africa. Aft. Entomol., 1: 175-182. Hoffmann, J.H. and Moran, V.C., 1991. Biological control of Sesbania punicea (Fabaceae) in South Africa. Agric. Ecosyst. Environ., 37: 157-173. Jaeger, P.-M.L. and Hepper, F.N., 1986. A review of the genus Solanum in Africa. In: W.G. D'Arcy (Editor), Solanaceae Biology and Taxonomy. Columbia University Press, New York, pp. 41-55. Neser. S., 1984. Report on a visit to Australia, Texas and Canada and countries en route with observations on biological control of weeds. Unpublished Report, Plant Protection Research Institute, Department of Agriculture and Water Supply, Pretoria, pp. 18-27. Neser, S., Zimmermann, H.G., Erb, H.E~ and Hoffmann, J.H., 1990. Progress and prospects for the biological control of two Solanum weeds in South Africa. In: E.S. Delfosse (Editor), Proc. 7th Int. Congr. Biological Control of Weeds, 1988, Rome, Italy, Inst. Sperimentale per la Patologia Vegetale Ministero dell'Agricoltura e delle Foreste, Rome, pp. 371-381. Olckers, T. and Hulley, P.E., 1989. Insect herbivore diversity on the exotic weed Solanum mauritianum Scop. and three other Solanum species in the eastern Cape. J. Entomol. Soc. South. Afr., 52:81-93. Olckers, T. and Hulley, P.E., 1991a. Impoverished insect herbivore faunas on the exotic bugweed Solanum mauritianum Scop. relative to indigenous Solanum species in Natal/KwaZulu and the Transkei. J. Entomol. Soc. South. Air., 54: 39-50. Olckers, T. and Hulley, P.E., 1991b. Seed damage by three local Heteroptera species on the exotic weed Solanum elaeagnifolium Cav. (Solanaceae). J. Entomol. Soc. South. Afr., 54: 269-270.
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Olckers, T. and Hulley, P.E., 1991c. Notes on some insect galls associated with Solanum plants in South Africa. S. Aft. J. Zool., 26: 55-61. Olckers, T. and Hulley, P.E., 1994. Resolving ambiguous results of host-specificity tests: the case of two Leptinotarsa species (Coleoptera: chrysomelidae) for biological control of Solanum elaeagnifolium cavanilles (Solanaceae) in South Africa. Afr. Entomol., 2: 137-144. Olckers, T. and Zimmermann, H.G., 1991. Biological control of silverleaf nightshade, Solanum elaeagnifolium, and bugweed, Solanum mauritianum (Solanaceae), in South Africa. Agric. Ecosyst. Environ., 37:137-155. Pearce, K., and Lester, R.N., 1979. Chemotaxonomy of the cultivated eggplant--a new look at the taxonomic relationships ofSolanum melongena L. In: J.G. Hawkes, R.N. Lester and A.D. Skelding (Editors), The Biology and Taxonomy of the Solanaceae. Academic Press, London, pp. 615-628. Siebert, M.W., 1975. Candidates for the biological control of Solanum elaeagnifolium Car. (Solanaceae) in South Africa. 1. Laboratory studies on the biology of Gratiana lutescens (Bob.) and Gratiana paUidula (Bob.) (Coleoptera: Cassidinae). J. Entomol. Soc. South. Aft., 38: 297304. Symon, D.E., 1981. A revision of the genus Solanum in Australia. J. Adelaide Bot. Gard., 4: 1-367. Wapshere, A.J., 1988. Prospects for the biological control of silver-leaf nightshade, Solanum elaeagmfolium, in Australia. Aust. J. Agric. Res., 39: 187-197. Zimmermann, H.G., 1974. Preliminary work on the biological control of satansbos, Solanum elaeagnifolium Cav. Unpublished Proceedings 1st National Weeds Conference, Pretoria, pp. 151-168.
Agriculture, Ecosystemsand Environment 52 ( 1995 ) 179-185
Importance of preintroduction surveys in the biological control of Solanum weeds in South Africa T. Olckers a'*, P.E. Hulley b aPlantProtectionResearch Institute, Private Bag X9059, Pietermaritzburg3200, South Africa bDepartment of Zoology and Entomology, Rhodes University, Grahamstown 6140, South Africa Accepted 31 May 1994
Abstract
Three exotic Solanum weeds, Solanum elaeagnifolium Cav., Solanum mauritianum Scop. and Solanum sisymbriifolium Lam. (Solanaceae), are targets for biological control in South Africa. Preintroduction surveys of the insect herbivores attacking these, as well as native and cultivated species of Solanum, have proved useful in several ways. Although there is a diverse, mainly oligophagous, herbivore fauna on native Solanum spp., that of the exotic weeds is mainly polyphagous and low in diversity and numbers. Feeding niches on introduced weeds are either vacant or underutilized, ensuring a wide scope for the selection of exotic biocontrol agents. Similarities between potential agents and native Solanum herbivores suggest that the former may recruit native parasitoids, a fact that has to be considered in the selection process. The surveys also helped to resolve a conflict of interest, caused by most candidate agents accepting the introduced crop plant Solanum melongena L. (eggplant) in specificity tests. Although a number of native Solanum oligophages attacked neglected eggplant fields, damage to crops is precluded by the pesticide regimes aimed at several generalist pests. Imported agents are no more a risk than native Solanum feeders, which are not regarded as pests. The surveys support the view that exotic agents should be introduced to control Solanum weeds.
Keywords: Biologicalcontrol; Solanaceae;South Africa
1. Introduction The exotic Solanum elaeagnifolium Cav. (silverleaf nightshade) and Solanum mauritianum Scop. (bugweed) are major weeds in South Africa, with the minor weed Solanum sisymbriifolium Lam. (wild tomato) becoming increasingly important. S. elaeagnifolium is native to the southwestern USA, Mexico and South America, and S. mauritianum and S. sisymbriifolium orig* Corresponding author.
inate from South America (Symon, 1981 ). South Africa has about 50 native and two cultivated Solanum spp. (Gibbs Russell et al., 1987). Of the latter, Solanum tuberosum L. (potato) is cultivated extensively in South Africa and Solanum melongena L. (eggplant, brinjal) is a crop of lesser importance (Annecke and Moran, 1982). The importance of biological control in the management of exotic Solanum weeds was reviewed by Olckers and Zimmermann ( 1991 ). Preintroduction surveys of the herbivores of exotic, native and cultivated Solanum spp. were
0167-8809/95/$09.50 © 1995 Elsevier Science B.V. All rights reserved SSDI 0167-88090 ( 94 ) 00537-0
180
T. Olckers, P.E. Hulley / Agriculture, Ecosystems and Environment 52 (1995) 179-185
undertaken in South Africa to determine: ( 1) the diversity of herbivore species on native Solanum spp. and the extent to which these may be preadapted to exotic species, (2) the biology, host range and relationships of the native herbivores, which could influence their feeding on exotic Solanum spp., (3) the numbers and impact of native herbivores attacking introduced weedy and cultivated species, (4) whether any potential biocontrol agents had already entered the country accidentally, as occurred for Trichapion lativentre (Brguin-Billecocq), a successful control agent ofSesbania punicea (Cav.) Benth. (Hoffmann and Moran, 1991 ), and (5) the taxonomic and ecological similarities between native herbivores and exotic agents to determine the extent to which native parasitoids may transfer to imported hosts.
2.2. Impact of native parasitoids on imported agents A field colony of an undescribed species of Frumenta (Gelechiidae), on an experimental plot of S. elaeagnifolium at the Uitenhage Weed Laboratory ( 33 ° 43'S; 25 ° 26'E), permitted observations on the impact of native parasitoids on imported American agents. These observations provided evidence to support predictions based on the results of the surveys. The plot comprised a 2 m × 2 m stand of plants on which 570 neonate caterpillars were placed on flowerbuds and budless shoots, where they formed seedless fruit and stem galls respectively. The neonates were released between November 1989 and January 1990 and survival was monitored by counts of galls and emerged moths. The galls were removed and dissected at the end of May 1990, when the plants senesced.
2. Methods 3. Herbivores on native Solanum spp.
2.1. Faunistic surveys Insect herbivores were collected on all exotic, native and cultivated Solanum spp. encountered in the eastern Cape Province, Transvaal and Natal regions of South Africa, between 1985 and 1992. During each collection, 10-20 plants were scanned for ectophagous herbivores in the field and representative samples were taken for further examination. Stems were dissected for borers and the foliage was scrutinized for 'cryptic' ectophages and other endophages. Fruit and flowers were also collected, one half being frozen for subsequent dissection and the remainder kept in emergence cages to allow for any immature herbivores or parasitoids to complete development. Immature stages of ectophagous herbivores were also kept in emergence cages for the same reason. Only insects feeding or reproducing on the plants were recorded. Voucher specimens of insect herbivores and parasitoids were placed in the Albany Museum (Grahamstown) and in the National Collection of Insects (Pretoria). The results of each regional survey were presented by Olckers and Hulley ( 1989, 1991a, 1994) and Hill et al. (1993).
Native Solanum spp. were attacked by a diverse insect herbivore fauna (Olckers and HulTable 1 Diversity of insect herbivores on exotic, cultivated and native species of Solanum in South Africa
Solanum species
Number of herbivore species a Spec.
Genr.
Total
Rank b
12 5
9 17
21 22
6 8
2
10
12
9
17
11
28
3
27 22 16 15
28 15 17 5
55 37 38 20
1 2 4 5
8
7
15
7
Exotic
S. elaeagnifolium S. mauritianum S. sisymbriifolium Cultivated
S. melongena Native
S. panduriforme S. incanum S. linnaeanum S. coccineum S. rigescens
a Specialists (Spec.) are insects specific to the genus Solanum; generalists (Genr.) attack plant families other than Solanaceae. b According to diversity of specialist herbivore species.
T. Olckers, P.E. Hulley / Agriculture, Ecosystems and Environment 52 (1995) 179-185
181
C h e w e r s ~ (37)
Suckers ~25)
Fruit-feeders
~
/
/
n-
ii!ill
\
\
~.
"~..'~ Flower-feeders ,3) "~'.. "..~/ L e a f - miners t2) \~.v^ ~ / ~all- formers
5
14)
4 NATIVE PLANTS
i!ilii i:?i: :i:i:! !:?i: iiili! i!iiii iiiiil
~i!iiii iiiiii
~iiiiiiilili!
ili~i "
?!:!: :i:i:i i!iiii
~i!i!ii ~i:!:i ii!~i~ :i:!:i ?i:? iiiii!
iiii!i +:<
~ii:/ii] iiiii~
o i!iili :i:!:i
Chewers
/ : ~ \ Fruit(5~eeders
,1,, /
2 E
\
~
Flowe~-feeders
-=1
(18)
I
2 EXOTIC PLANTS
I
,
4
5
Number
I
6
l
7
l
8
9
H 10
of host plants
Fig. 2. Number of host plant species recorded for common insect herbivores associated with native Solanum spp. in South Africa.
Ch~,ers
,1,,
3
iilii! :i:!:! iiiiii :i:!:i !:i:i: i!iiii
\ 12>
CULTIVATED PLANTS
Fig. I. Insect herbivores associated with native, exotic and cultivated Solanum spp. in South Africa. Endophagous guilds are indicated by shaded sectors; numbers of insect species per group are indicated in parentheses. Plant categories as in Table 1.
ley, 1989, 1991a; Table 1), comprising many species that occurred over a wide geographic range and appeared to be specific to the genus Solanum. These specialist species constituted potential colonists, from which potentially preadapted species might attack introduced Solanum spp. In addition, a number of generalists, some of which were consistently associated with the genus, contributed to the often high levels of damage. The guild structure of the herbivore "pool' (Fig. 1 ) showed a predominance of chewing and sucking ectophagous species. The endophagous species (27% of the community) included stemborers, gall-formers, leaf-miners, fruit-feeders and flower-feeders. Native Solanum herbivores thus have representatives in all major guilds. Of the specialist herbivores (i.e. those specific
to the genus), 75% occurred on at least three host Solanum spp. (Fig. 2 ), indicative of oligophagy. This, and the number of generalist species (2558% of native Solanum herbivores; Table l ), made preadaptation to feeding on exotic Solanum spp. very likely.
4. Role of native insects in Solanum biocontrol
Exotic plants may be damaged by herbivores of native plants when these include close relatives (e.g. exotic thistles (Asteraceae) in the USA (Goeden, 1971, 1974; Goeden and Ricker, 1986 ) ). However, the three exotic Solanum spp. had few, largely generalist, herbivores (Table 1 ) and were relatively undamaged in comparison to native plants (Olckers and Hulley, 1989, 1991 a; Hill et al., 1993). No trace was found of any accidentally introduced herbivores. Twelve specialist species were recorded on S. elaeagnifolium, five on S. mauritianum and two on S. sisymbriifolium (Table 1 ), but in low numbers and causing only minor damage. Exotic species differed from native plants (Fig. 1 ) in having no gall-formers or leaf-miners. Endophages comprised 18% of the community, although 71% were
182
72. OIckers, P.E. Hulley / Agriculture, Ecosystems and Environment 52 (1995) 179-185
Table 2 Similarities between candidate agents for S. elaeagnifolium and native Solanum insectsa Candidate agent
Native insectsb
Parasitoids c
Gratiana spp. (D) (Chrysomelidae: Cassidinae )
Conchyloctenia spp. (D) (Chrysomelidae: Cassidinae)
1 sp. (egg) 2 spp. (pupal)
Leptinotarsa spp. (D) (Chrysomelidae: Chrysomelinae )
Conchyloctenia spp. (D) (Chrysomelidae: Cassidinae ) Epilachna spp. (D) (Coccinellidae)
Asabove
Frumenta nephelomicta ( FG ) (Gelechiidae)
Scrobipalpa concreta ( FG ) (Gelechiidae)
4 spp. (larval)
Frumenta sp. (FG/SG) (Gelechiidae)
Scrobipalpa concreta ( FG ) Unidentified sp. (SG) Scrobipalpa incola ( SG ) (All Gelechiidae )
As above 4 spp. (larval) 2 spp. (larval)
Trichobaris texana ( SB ) (Curculionidae)
Oberea trigonalis (SB) (Cerambycidae) Pseudagrilus sp. (SB) (Buprestidae)
Unknown
Carpophilus sp. (FL) (Nitidulidae)
Pria sp. (FL) (Nitidulidae)
Unknown
Symmetrischema ardeola (FL ) (Gelechiidae)
Scrobipalpa concreta ( FG ) (Getechiidae)
4 spp. (larval)
Unidentified sp. (SG) (Cecidomyiidae)
Unidentified sp. (LG) (Cecidomyiidae)
10 spp. (larval)
Anthonomus sp. (FL) (Curculionidae)
Pria sp. (FL) (Nitidulidae)
Unknown
Gargaphia arizonica (D ) (Tingidae)
Urentius hystricellus (D) (Tingidae)
Unknown
Zonosemata vittigera ( FR ) (Tephritidae)
Silba ophyroides (FR ) (Lonchaeidae) Atherigona orientalis (FR ) (Muscidae)
Unknown
2spp.(pupal)
Unknown
Unknown
a D, defoliators; SB, stem-borers; SG, stem-gallers; FL, flower-feeders; FG, flower-gallers; FR, fruit-feeders; LG, leaf-gallers. b Either close relative and/or with similar biology. c Parasitoids of native Solanum insects are indicated. polyphagous fruit-feeders and thus not part o f the regular S o l a n u m h e r b i v o r e 'pool'. In S. e l a e a g n i f o l i u m 57%, in S. m a u r i t i a n u m 23% a n d in S. s i s y m b r i i f o l i u m 17% o f the herbivores originated f r o m the native S o l a n u m herbivore 'pool', the rest being generalist species
(Table 1 ). This reflects the fact that S. elaeagnif o l i u m belongs to the s a m e subgenus as the native species a n d has close relatives a m o n g s t the native plants, whereas S. m a u r i t i a n u m belongs to a subgenus o f S o l a n u m which is not represented in Africa ( D ' A r c y , 1972; Jaeger a n d H e p -
T. Olckers, P.E. Hulley / Agriculture, Ecosystems and Environment 52 (1995) 179-185
per, 1986). S. sisymbriifolium, however, belongs to the same subgenus as native species but is much more heavily endowed with glandular trichomes, which rarely occur on native species (Hill et al., 1993). The exotic Solanum spp. are underexploited so far as their defences are probably unique, and herbivores of native Solanum spp. are not preadapted to overcome them. The only insects inflicting appreciable damage were polyphagous hemipterans which caused sporadic seed mortality of 46-67% on S. elaeagnifolium (Olckers and Hulley, 1991b). Native insects are unlikely to contribute much to the control of the three weeds, leaving wide scope for selecting exotic biological control agents.
5. Impact of native parasitoids on imported agents Native predators and parasitoids often interfere with agents imported for weed control, often preventing establishment. According to Goeden and Louda (1976), predators involved were mainly polyphagous, with parasitoids often transferring from closely related native herbivores. The preintroduction surveys showed that South African Solanum faunas included many herbivores with taxonomic and ecological similarities to potential agents from the Americas, which increased the chances for parasitoids to attack them. This was particularly true of agents for S. elaeagnifolium (cf. Table 2 and Zimmermann, 1974; Neser, 1984; Wapshere, 1988). The surveys provided the opportunity to rear and identify parasitoids and there is evidence to predict that many candidate agents for S. elaeagnifolium would rapidly be parasitized in South Africa. Laboratory studies on American tortoise beetles (Gratiana spp.) indicated that pupae were susceptible to eulophid parasitoids of tortoise beetles (Conchyloctenia spp.) associated with native Solanum spp. (Siebert, 1975 ). Field observations on the American fruit- and stemgalling gelechiid (Frumenta sp.) revealed that moths emerged from only 14% of the galls initially formed. Although mortality was also caused
183
by desiccation of early instars and moths failing to emerge properly, 51% of mortality could be attributed to parasitism. The parasitoids were not identified because galls were dissected after they had emerged. However, they were most likely parasitoids of three gelechiid moths which form galls on at least six native Solanum spp. (Table 2; Olckers and Hulley, 1991 c). On the other hand, defoliating Leptinotarsa spp. (Chrysomelinae), whose closest native relatives are Conchyloctenia spp. (Cassidinae), are less likely to attract native parasitoids. Leptinotarsa larvae are unique in that they pupate underground and are also larger, more active and quicker in development than Conchyloctenia spp., in which parasitism is concentrated on the egg stage. Eggs of Leptinotarsa spp. may be vulnerable, but are morphologically similar to those of native Epilachna spp. (Coccinellidae) from which no parasitoids were reared. Leptinotarsa spp. are therefore considered the most promising biocontrol candidates for S. elaeagnifolium (Olckers and Zimmermann, 1991 ). Other agents, like Trichobaris texana LeConte and Anthonomus sp., which have no close relatives among herbivores of native Solanum spp. (Table 2), may thus also be suited for release on S.
elaeagnifolium. 6. Suitability of agents for release According to Annecke and Moran (1982), pests of introduced solanaceous crops such as potatoes ( S. tubersum ), tomatoes ( Lycopersicon spp.), peppers (Capsicum spp.), eggplant (S. melongena ) and tobacco (Nicotiana tabacum L. ) are mostly polyphagous species. Recruitment of native Solanum herbivores thus appears negligible in South Africa, as for exotic Solanum weeds. However, the present surveys indicate a far greater diversity of insects injurious to eggplant than reported in the literature (Olckers and Hulley, 1994). Field crops were attacked by 28 insect species, 61% of which were specialists from the Solanum herbivore 'pool' (Table 1 ). Some of them caused considerable damage in the absence of the usual pesticide regimes. The ease
184
T. Olckers, P.E. Hulley / Agriculture, Ecosystems and Environment 52 (1995) 179-185
with which native herbivores feed on eggplant was exemplified by a leaf-galling cecidomyiid, previously recorded on one native Solanum species only (Olckers and Hulley, 1991 c ). Virtually all groups of herbivores associated with native Solanum spp. were represented on eggplant (Fig. 1 ) and endophages comprised 29% of the community. These results reflect the fact that eggplant is very closely related to some native Solanum spp. (D'Arcy, 1972; Pearce and Lester, 1979). Eggplant may lack chemical defences, because of selection for palatability, or else may have defences very similar to that of native species which native herbivores have already overcome. These findings also imply that imported agents could transfer to poorly defended Solanum crops like eggplant. Indeed, this occurred during specificity tests with four promising species of Gratiana and Leptinotarsa (Chrysomelidae); although solanaceous crops like potatoes, tomatoes, peppers and tobacco were unacceptable to them, they all fed and survived on eggplant (Neser et al., 1990; Olckers and Zimmermann, 1991 ); yet none of these candidates are known to attack eggplant on the American continent (Neser et al., 1990; Olckers and Zimmermann, 1991 ). However, the readiness with which many of the native Solanum herbivores attacked eggplant suggests that imported agents could do so during stress situations, as they did in the laboratory. Biocontrol of Solanum weeds in South Africa had thus reached a stalemate in that releases of agents were perceived as risky. The preintroduction surveys revealed that eggplant cultivations are protected from generalists (e.g. spider mites, lepidopterous larvae, aphids ) by a range of broad-based pesticides (e.g. monocrotophos, deltamethrin, endosulphan). Although highly toxic chemicals (e.g. monocrotophos, profenofos) were applied as required, most pesticides were, on average, applied once every 2 weeks. It was clear that these severe pesticide regimes also completely protected eggplant from native Solanum oligophages, to the extent that they are not regarded as pests (cf. Annecke and Moran, 1982; Olckers and Hulley, 1994). Furthermore, chemical trials (Olckers and Hulley, 1994) indicated that the more common pes-
ticides were lethal to Leptinotarsa spp. and should thus prevent any agents that might move onto eggplant from persisting. These lines of evidence suggest that imported agents are no more a threat than native insects. We therefore argue that imported insects could be released to control Solanum weeds, in spite of the apparent presence of a crop at risk.
Acknowledgements The authors thank G.B. Dennill, R.L. Kluge and anonymous referees for comments on the manuscript. The senior author is grateful to The Anglo American and De Beers Chairman's Fund for a travel grant which enabled him to present this work at the VIII International Symposium on Biological Control of Weeds, held at Lincoln University, New Zealand.
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T. Olckers, P.E. Hulley / Agriculture, Ecosystems and Environment 52 (1995) 179-I85 vanilles and S. sisymbriifolium Lamarck (Solanaceae) in South Africa. Aft. Entomol., 1: 175-182. Hoffmann, J.H. and Moran, V.C., 1991. Biological control of Sesbania punicea (Fabaceae) in South Africa. Agric. Ecosyst. Environ., 37: 157-173. Jaeger, P.-M.L. and Hepper, F.N., 1986. A review of the genus Solanum in Africa. In: W.G. D'Arcy (Editor), Solanaceae Biology and Taxonomy. Columbia University Press, New York, pp. 41-55. Neser. S., 1984. Report on a visit to Australia, Texas and Canada and countries en route with observations on biological control of weeds. Unpublished Report, Plant Protection Research Institute, Department of Agriculture and Water Supply, Pretoria, pp. 18-27. Neser, S., Zimmermann, H.G., Erb, H.E~ and Hoffmann, J.H., 1990. Progress and prospects for the biological control of two Solanum weeds in South Africa. In: E.S. Delfosse (Editor), Proc. 7th Int. Congr. Biological Control of Weeds, 1988, Rome, Italy, Inst. Sperimentale per la Patologia Vegetale Ministero dell'Agricoltura e delle Foreste, Rome, pp. 371-381. Olckers, T. and Hulley, P.E., 1989. Insect herbivore diversity on the exotic weed Solanum mauritianum Scop. and three other Solanum species in the eastern Cape. J. Entomol. Soc. South. Afr., 52:81-93. Olckers, T. and Hulley, P.E., 1991a. Impoverished insect herbivore faunas on the exotic bugweed Solanum mauritianum Scop. relative to indigenous Solanum species in Natal/KwaZulu and the Transkei. J. Entomol. Soc. South. Air., 54: 39-50. Olckers, T. and Hulley, P.E., 1991b. Seed damage by three local Heteroptera species on the exotic weed Solanum elaeagnifolium Cav. (Solanaceae). J. Entomol. Soc. South. Afr., 54: 269-270.
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Olckers, T. and Hulley, P.E., 1991c. Notes on some insect galls associated with Solanum plants in South Africa. S. Aft. J. Zool., 26: 55-61. Olckers, T. and Hulley, P.E., 1994. Resolving ambiguous results of host-specificity tests: the case of two Leptinotarsa species (Coleoptera: chrysomelidae) for biological control of Solanum elaeagnifolium cavanilles (Solanaceae) in South Africa. Afr. Entomol., 2: 137-144. Olckers, T. and Zimmermann, H.G., 1991. Biological control of silverleaf nightshade, Solanum elaeagnifolium, and bugweed, Solanum mauritianum (Solanaceae), in South Africa. Agric. Ecosyst. Environ., 37:137-155. Pearce, K., and Lester, R.N., 1979. Chemotaxonomy of the cultivated eggplant--a new look at the taxonomic relationships ofSolanum melongena L. In: J.G. Hawkes, R.N. Lester and A.D. Skelding (Editors), The Biology and Taxonomy of the Solanaceae. Academic Press, London, pp. 615-628. Siebert, M.W., 1975. Candidates for the biological control of Solanum elaeagnifolium Car. (Solanaceae) in South Africa. 1. Laboratory studies on the biology of Gratiana lutescens (Bob.) and Gratiana paUidula (Bob.) (Coleoptera: Cassidinae). J. Entomol. Soc. South. Aft., 38: 297304. Symon, D.E., 1981. A revision of the genus Solanum in Australia. J. Adelaide Bot. Gard., 4: 1-367. Wapshere, A.J., 1988. Prospects for the biological control of silver-leaf nightshade, Solanum elaeagmfolium, in Australia. Aust. J. Agric. Res., 39: 187-197. Zimmermann, H.G., 1974. Preliminary work on the biological control of satansbos, Solanum elaeagnifolium Cav. Unpublished Proceedings 1st National Weeds Conference, Pretoria, pp. 151-168.