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The Herbivores of Solanum carolinense (Horsenettle) in Northern Virginia: Natural History and Damage Assessment
Michael J. Wise

Southeastern Naturalist, Volume 6, Number 3 (2007): 505–522

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2007 SOUTHEASTERN NATURALIST 6(3):505–522 The Herbivores of Solanum carolinense (Horsenettle) in Northern Virginia: Natural History and Damage Assessment Michael J. Wise* Abstract - I studied interactions between the herbaceous weed Solanum carolinense (horsenettle) and its herbivore community in northern Virginia from 1996–2002. Thirty-two species regularly fed on the plant, including 31 insects from 6 taxonomic orders and Microtus pennsylvanicus (meadow vole). An intensive field experiment on 960 horsenettle individuals in 2001 revealed high levels of damage to all parts of the plants. Two chrysomelid beetles—Epitrix fuscula (eggplant flea beetle) and Leptinotarsa juncta (false potato beetle)—damaged leaves on nearly every plant. Roughly half of the flowers were destroyed by herbivores, with Anthonomus nigrinus (potato bud weevil) destroying 30%. Nearly three-fourths of the fruits were damaged by three species: the tephritid fly Zonosemata electa (pepper maggot), false potato beetle, and meadow vole. The weevil Trichobaris trinotata (potato stalk borer) bored in stems of 73% of the plants, and the most damaging root feeder was the moth Synanthedon rileyana (Riley’s clearwing). A literature review on the horsenettleherbivore community is integrated with new observations as a guide for applied and basic research on this economically significant species. Introduction Solanum carolinense L. (Solanaceae) (horsenettle) is a perennial herbaceous plant native to the southeastern United States. It has expanded its range northward to Ontario and westward to California, and it has become an invasive weed in temperate and tropical areas in Europe and Asia (Ilnicki et al. 1962, Imura 2003, NAPPO 2003). Horsenettle reproduces vegetatively through a rapidly expanding root system, and sexually through flowers and fruits (Ilnicki et al. 1962). Racemes mature from base to tip and may bear 1 to over 20 flowers (mean 􀂧 8). Horsenettle blooms in Virginia from late May until early October. Mature fruits are round, yellow berries with an average diameter of 1.5 cm. Several species of birds and mammals have been reported to feed on horsenettle fruits (Bassett and Munro 1986, Cipollini and Levey 1997b, Martin et al. 1951). Nevertheless, it is common for many fruits to remain on horsenettle plants throughout the winter, indicating that seed dispersal may be suboptimal. Horsenettle has traits that are likely to function as herbivore deterrents, including spines, stellate trichomes, and a variety of secondary chemicals, especially toxic alkaloids (Bassett and Munro 1986, Ilnicki et al. 1962, Nichols et al. 1992, Thacker et al. 1990). Despite these potential defenses, horsenettle is subject to feeding by numerous herbivores, and no part of the plant is immune to attack. *Department of Biology, Duke University, Durham, NC 27708. Current address - Department of Biology, Bucknell University, Lewisburg, PA 17837; mwise@bucknell.edu. 506 Southeastern Naturalist Vol. 6, No. 3 Horsenettle is one of the most significant weeds in the eastern United States. It is an economically important pest of grain and fruit crops (Banks et al. 1977, Bassett and Munro 1986, Frank 1990, Hackett et al. 1987, Prostko et al. 1994) and is toxic to livestock (Bassett and Munro 1986, Gorrell et al. 1981). Horsenettle may have an indirect adverse impact on solanaceous crop plants (e.g., eggplants, potatoes, tomatoes, and peppers) by serving as a wild reservoir for insect pests (Aguilar and Servín 2000, Burke 1976, Faville and Parrott 1899, Foott 1968, Ilnicki et al. 1962, Judd et al. 1991, Mena-Covarrubias et al. 1996). Any efforts to use biological control against horsenettle (and efforts to control pest insects that horsenettle shares with crop plants) must be based on a sound knowledge of the herbivore community and the type and amount of damage they inflict. In addition to its agricultural significance, horsenettle and its herbivores are increasingly being used as study species by ecologists and evolutionary biologists. This system has been used to address topics such as the impact of herbivores on plant fitness (Solomon 1983; Wise and Cummins 2002, 2006; Wise and Sacchi 1996), plant defensive chemistry (Cipollini and Levey 1997a, b; Cipollini et al. 2002a; Thacker et al. 1990), interspecific competition among herbivores (Cipollini et al. 2002b, Wise and Weinberg 2002), and maternal care in subsocial insects (Hardin and Tallamy 1992, Loeb 2003). Horsenettle has been the focus of studies on the evolution of sexallocation strategies and self-incompatibility systems (Elle 1998, 1999; Elle and Meagher 2000; Richman et al. 1995; Solomon 1985, 1986; Steven et al. 1999; Stone 2004, Uyenoyama 1997; Vallejo-Marín and Rausher, in press). As with applied research, the conclusions of ecological and evolutionary studies will be stronger if interpreted within the context of the whole community of horsenettle herbivores. Despite the applied and basic interest in horsenettle and its herbivores, a comprehensive overview of the plant’s native herbivore community is not available. To fill this need, I report here on observations from 7 years of research in northern Virginia. This paper has 3 specific objectives: (1) provide a comprehensive list of horsenettle herbivores within the plant’s native range; (2) report on a study of the magnitude of damage imposed by herbivores; and (3) integrate new natural history information with older literature on the herbivores. Methods Study area From 1996–2002, I performed a series of observational and experimental studies of horsenettle and its community of herbivores in old fields in and around Blandy Experimental Farm (Shenandoah Valley at 39ºN, 78ºW, Clarke County, VA). Blandy Farm receives an average of 94 cm of rain per year. 2007 M.J. Wise 507 Field experiment setup In the spring of 1997, I collected root material from 30 horsenettle plants (i.e., genets) growing at least 10 m apart along transects in each of 4 populations within a 13-km radius of Blandy Farm. Plants were propagated in pots in commercial growing media (Wesco Growing Media III, Wetsel Seed Company, Harrisonburg, VA) each year through 2002. Propagation procedures may be found in Wise (2003). In early May of 2001, I cut roots from plants of 40 different genets (10 from each of the 4 source populations) into 2-cm3 segments. I planted at least 38 segments from each of the 40 genets individually in growing media in 3.8-liter (1-gallon) pots. Between 28 June and 2 July of 2001, I chose 24 ramets (individual stems) from each of these 40 genets and transplanted them into an old agricultural field at Blandy Farm that already had an extensive population of horsenettle. These 960 ramets were planted in a randomized block design with 3 spatial blocks, each consisting of 10 rows separated by 2 m. Each row contained 32 ramets spaced 1.5 m apart, and the ramets were flagged and labelled with plastic tags in the soil. The growing media from the pot of each ramet was covered with a layer of field soil and dead grass from the field so that the transplanted plants would blend with native horsenettles. The density of horsenettle in the field before transplantation was approximately 12 ramets per m2; thus, the ratio of native to transplanted ramets within experimental blocks was about 30:1. Field experiment data collection Data collection on floral herbivory began immediately after transplanting and continued until flowering ceased in late September. Each plant was checked every 3–5 days, and the fate of each flower was recorded as either aborted in the bud stage unrelated to herbivory, killed by one of several herbivore species, or successfully opened. Fruit abortion, maturation, and herbivory were also noted throughout the growing season. Each raceme was collected once its fruits started ripening (before they could be dispersed); fruits were kept in plastic bowls in a growth chamber to rear out insects. After the emergence period, I dissected each fruit to search for additional evidence of feeding. A series of hard freezes from 8–10 October killed all stems and stopped development of fruits. I was unable to identify any insects that may have been in these unripe fruits at the time of this frost. Data on leaf herbivory were taken in 2 cycles, corresponding to the peaks in damage by folivores. In August, I measured damage by Epitrix fuscula (eggplant flea beetles), Leptinotarsa juncta (false potato beetles), and Tildenia inconspicuella (eggplant leafminers) (see Appendix 1 for insect nomenclature). In early September, I measured damage by Gratiana pallidula (eggplant tortoise beetles), Gargaphia solani (eggplant lace bugs), and Prodiplosis longifila (citrus gall midges). The presence of other species of herbivores was noted each time the plants were checked. Here, I report 508 Southeastern Naturalist Vol. 6, No. 3 only the proportion of the 960 plants that displayed damage by folivores. Details of the methods used to quantify the damage more specifically for each species may be found in Wise (2003). I harvested stems down to the roots once plants had senesced, beginning on 30 September and ending after the killing October frosts. I dissected each stem to collect insects and note signs of stem boring. Results and Discussion Overview of herbivore damage From 1996–2002, I documented 31 species of insect herbivores that regularly feed on horsenettle, including members of 6 taxonomic orders (Table 1, Appendix 1). The only non-insect herbivore was Microtus pennsylvanicus (Ord) (Cricetidae: Arvicolinae) (meadow vole). A variety of feeding modes were utilized by these insects, including chewing, piercingand- sucking, leaf mining, galling, and stem boring. The herbivores ranged from horsenettle specialists, such as the moth Frumenta nundinella and the Table 1. Geographic ranges of 11 major horsenettle herbivores in the US. Specific records are noted with state abbreviations. Herbivore species Geographic range in the US References Hemiptera Gargaphia solani AL AZ AR CT DC GA IA IL IN Henry and Froeschner (1988) KS MA MD MS MO NC NJ OH OK PA SC TN TX VA Coleoptera Leptinotarsa juncta Southern US; AR Fl IN LA NC Downie and Arnett (1996); OH PA VA Jaques (1951) Epitrix fuscula Eastern half of US; AL Fl IN NY Downie and Arnett (1996); OH OK Jaques (1951) Gratiana pallidula AZ CA Fl GA MD NY PA VA Downie and Arnett (1996) Anthonomus nigrinus AR CT DC GA IL IN KS KY LA Downie and Arnett (1996) MI MO MS NC NJ NY OK SC TN TX VA WV Trichobaris trinotata CO CT DC Fl IA IL IN KS MD Downie and Arnett (1996) MI MO MS NC NJ NY PA SC TX VA Diptera Prodiplosis longifila Fl Peña et al. (1989) Zonosemata electa AL CT DC Fl GA IA IL IN KS Foote et al. (1993) MD MO MS NJ NY SC TN TX WV VA Lepidoptera Tildenia inconspicuella AK AL DE Fl GA IA IL IN KS Gross (1986) KY LA MD MO NC NJ OK PA SC TX VA WV Frumenta nundinella Eastern US; AK GA IL IN MO Bailey and Kok (1982) PA TX VA Mammalia Microtus pennsylvanicus East of Rocky Mountains, south Maser and Storm (1970 to NM and GA 2007 M.J. Wise 509 false potato beetle, to extreme generalists, such as the meadow spittlebug and the salt marsh caterpillar. In the field experiment, every type of plant organ was subject to attack by at least 1 and usually several different species. Leaves were attacked by the greatest diversity of herbivores, with 6 different species of folivores, each damaging at least 6% of the plants (Fig. 1A). Evidence of stem boring was found in 73% of the plants. Slightly fewer than half of the flowers and only about a quarter of all fruits (excluding those that aborted undamaged or were killed by frost) escaped or survived herbivory (Fig. 1B, C). About 10% of the fruits were destroyed by frost before maturing. Any insects that might Figure 1. Damage levels of major herbivores in an experimental population of 960 horsenettle ramets. A. Leaf herbivory: % of ramets displaying leaf damage. B. Floral herbivory. The “other herbivores” include eggplant flea beetles, eggplant tortoise beetles, tobacco hornworms, and an unidentified microlepidopteran. The fates of 2% of flowers were unknown. C. Fruit herbivory. The “other herbivores” include potato bud weevils and tobacco hornworms. The “aborted” fruits only include those that did not receive any damage. The “frost damaged” fruits may have been infested by pepper maggots, but maggots were destroyed by hard freezes along with unripe fruits. 510 Southeastern Naturalist Vol. 6, No. 3 have been in these fruits were also destroyed, along with evidence of their feeding. Almost 15% of the fruits aborted before the frosts without showing any evidence of herbivore damage. Leaf-feeding herbivores Eggplant flea beetle. This small, black beetle was the most ubiquitous herbivore species in this study. Adults feed by chewing trichomes off a small area of a leaf, consuming leaf tissue that was under the trichomes, and then moving to a new area of the leaf or a different leaf. Their feeding results in a distinctive shotgun pattern of small holes in a leaf’s surface. This leaf damage may be severe, and no horsenettle plant (and virtually no leaf) in the field experiment escaped flea beetles entirely. Adults may be found from the time of horsenettle emergence in the spring until the first killing frost in the fall. Larvae feed on horsenettle roots and cause relatively mild damage compared to adults. While I occasionally encountered other species of Epitrix on horsenettle, eggplant flea beetles were by far the most abundant. False potato beetle. This congener of the infamous L. decemlineata (Colorado potato beetle) has also been referred to as the horsenettle beetle or the false Colorado potato beetle (Jacques 1988). The false potato beetle, which is a specialist on horsenettle, is found throughout the southeastern US (Hsiao 1986, Jacques 1988). Adult beetles emerge in late spring, coinciding with the emergence of horsenettle shoots. Bright orange eggs are laid in small clusters on the underside of horsenettle leaves or on nearby plants. Though they appear to be bivoltine in northern Virginia (Wise and Sacchi 1996), larvae may be found continuously until nearly the end of horsenettle’s growing season. Both adults and larvae feed mainly on leaves, chewing from the edges toward the midveins. Larvae often feed in groups, which may help them to overcome the physical toughness of the leaves (Hsiao 1986). These beetles may also cause considerable damage to horsenettle flowers and developing fruits. Despite reports of feeding by the similar looking Colorado potato beetle on horsenettle in other geographic regions (Mena-Covarrubias et al. 1996), I rarely encountered Colorado potato beetle on horsenettle through the duration of this study. It has been reported that the extension of Colorado potato beetle's geographic range has caused a drastic decline in populations of false potato beetle, either because the former depleted its food source or interbreeding genetically swamped false potato beetles to near extinction (Jacques 1988). Experimental evidence argues against these reports (Neck 1983). For instance, Hare and Kennedy (1986) found that survival of Colorado potato beetle larvae from Virginia potato fields was extremely low on horsenettle, suggesting that the food sources of the 2 species overlap very little. In addition, Boiteau (1998) found that behavioral and gametic barriers prevent the 2 species from interbreeding. These findings, combined with the relative abundance of the beetles in this study, argue that the false potato beetle is not suffering from invasions by its infamous congener, at least in northern Virginia. 2007 M.J. Wise 511 Eggplant tortoise beetle. This species was the third most common chrysomelid beetle on horsenettle, with 42% of the ramets in the field experiment exhibiting tortoise beetle damage. Both larvae and adults feed almost exclusively on leaves, concentrating on the interior of the leaf surface, away from the leaf edges and between major veins. Their damage is easily distinguished as uniform oval-shaped holes, up to about 1 cm in length, depending on the size of the beetles. They were occasionally observed feeding on flower petals. Margined blister beetle. Adults of this beetle appear in horsenettle populations in mid-to-late summer. They tend to congregate in small groups, so their feeding damage is often localized. While they may damage some flowers, their feeding is concentrated on the lower, older leaves of horsenettle. These blister beetles feed from the edges of leaves like potato beetles, but they tend to avoid major veins, with the result that their leaf damage often appears in characteristic triangular segments. Because adults concentrate their feeding on older leaves near the end of the season and because larvae do not feed on horsenettle (they feed on grasshopper eggs), the margined blister beetle does not appear likely to have a serious impact on horsenettle fitness in this study area. Eggplant lace bug. Adults and nymphs feed by sucking contents from leaf parenchyma cells, causing yellowing and premature abscission of leaves (Loeb 2003). Most damage is caused by nymphs, which feed in groups of up to several hundred guarded by an adult female (Loeb et al. 2000). Eggplant lace bugs may have as many as 8 generations per year in Virginia (Tallamy and Denno 1982), and their densities may reach very high levels within a horsenettle population; thus, damage may be locally quite severe. However, these lace bugs also appear prone to population crashes. I have found that heavily damaged horsenettle populations may remain essentially free of lace bugs for several successive years. Citrus gall midge. Horsenettle is a new host record for the citrus gall midge, and before this study the species had not been reported north of Florida (Gagné 2004, Peña et al. 1989). Although this gall midge generally feeds on flowers (Gagné 1989), on horsenettle the larvae feed in rolled-up leaves, usually in terminal clusters at the plant’s apex or the end of an axillary shoot. The mature larvae drop from the plants and pupate in the soil. The citrus gall midge may be abundant in horsenettle populations in moist or shaded areas. When on plants in relatively open fields, the gall midges almost always occurred on leaves that were near the ground and shaded by other plants. Though the damage these gall midges do is small in terms of leaf area consumed, their impact on horsenettle fitness may be disproportionately large because their feeding often damages apical or axillary meristems, thus stunting plant growth. Eggplant leafminer. This gelechiid moth attacks horsenettle in multiple, overlapping generations from early summer until the first frost of autumn. Female moths deposit eggs singly on leaf surfaces, and larvae tunnel into the leaves, eventually forming a blotch mine from the edge of the leaves (Gross 512 Southeastern Naturalist Vol. 6, No. 3 1986). I have found between-year variation in population sizes of the eggplant leafminer to be substantial. At low leafminer population densities, it is relatively uncommon for more than 1 mine to occur on a leaf. At higher densities, multiple mines may occur on a single leaf, and several larvae may share a communal mine. Damaged leaf areas turn brown, curl up from the edges of the leaves, and may eventually fall off. This is the only species of leafminer I observed on horsenettle during the study period. Salt marsh caterpillar and tobacco hornworm. Larvae of two species of moths, Estigmene acrea (salt marsh caterpillar) and Manduca sexta (tobacco hornworm), were regularly, though not commonly, observed to feed on horsenettle throughout the study period. Salt marsh caterpillars generally feed on leaves, but they sometimes cause substantial damage to flowers. Large hornworm caterpillars sometimes strip entire horsenettle ramets of leaves, flowers, and developing fruits. In the transplant study, 5 of the 960 plants incurred measurable hornworm damage. Larvae and pupae of several species of tortricid moths were occasionally found on horsenettle, but none appeared to cause appreciable damage. Frumenta nundinella. This gelechiid moth has an unusual natural history. In the spring, female moths lay eggs near the apices of young horsenettle ramets (Bailey and Kok 1982). Upon hatching, a larva glues terminal leaves together to form a roughly spherical structure in which it feeds on the apical meristem (Solomon 1981). These structures, which reach a diameter of about 2 cm (Solomon 1983), are usually found at the plant apices, but they may be found as well on axillary meristems of larger plants. The insects pupate inside the structures, and adults emerge in early summer. The females of this generation generally lay their eggs on or near horsenettle flower buds (Solomon 1980). Once a larva enters a flower bud, a fruit begins to form parthenocarpically around the larva, perhaps in response to damage to the style, and the larva feeds on ovules of the unfertilized fruit (Solomon 1980). The infested fruits look relatively normal from the outside (though often a bit lumpy), but they usually contain no seeds, or at most a very few seeds. Prior to pupation, the larva chews an emergence hole in the side of its fruit, leaving a thin, membranous window (Solomon 1981). Pupation occurs within the fruits, and the second-generation adult moths emerge in the late summer. In the field study, larvae inside fruits were commonly parasitized by 2 species of wasps: Conura dema (Burks) (Chalcididae) and Bracon sp. (Braconidae). Foott (1967) recorded parasitism by Bracon mellitor Say on F. nundinella in fruits in Canada. Solomon and McNaughton (1979) reported that larvae in both leaf chambers and fruits were commonly parasitized by the wasp Scambus pterophori (Ashmead) (Ichneumonidae) in central New York, but this species was not observed in this study. Sap-feeding herbivores A number of homopteran sap feeders regularly attack horsenettle, including Aphididae (aphids), Cercopidae (spittlebugs), Cicadellidae (leafhoppers), Flatidae and Acanaloniidae (planthoppers), Membracidae 2007 M.J. Wise 513 (treehoppers), and Aleyrodidae (whiteflies). Adult Philaenus spumarius (meadow spittlebugs) were quite common on horsenettle throughout most of the plant’s growing season, but feeding by nymphs was extremely rare. Over the course of this study, I also observed numerous species of leafhoppers and planthoppers on horsenettle, but it was not always apparent whether they were actually feeding or just resting between stops on their host plants. The treehopper Entylia bactriana was commonly found feeding on the midveins of horsenettle leaves in the fall, particularly in populations near woodlots in years with a late killing frost. In most horsenettle populations, whiteflies also are not present until autumn. The later in autumn the first hard frost occurs, the more abundant whiteflies become. In years with especially late first frosts, virtually all horsenettle plants in some populations became heavily infested by whiteflies. I have also observed whiteflies on horsenettle in the middle of the summer, but only in isolated plant populations with very little damage from other herbivores. Flower-feeding herbivores Potato bud weevil. A rather inconspicuous black beetle, Anthonomus nigrinus (potato bud weevil),was the main floral herbivore of horsenettle. Overwintering adults begin to emerge in the spring in general synchrony with the sprouting of horsenettle ramets. Before flower buds are produced, the weevils can often be found congregating on horsenettle leaves. Adults will feed on leaves, but they seem to prefer flowers (Burke 1976). Most of the floral damage occurs, however, when females oviposit. A female chews a hole into a flower bud and oviposits onto an anther. She then plugs the hole with a fecal pellet and proceeds to chew the flower’s pedicel. Such flower buds either fall off immediately or die attached to the raceme and fall a few days later. Larvae feed and pupate inside the unopened flower buds. Development is rapid, sometimes lasting less than a month from egg to adult (Chittenden 1895). Usually 1, but up to 3 adults may emerge from a single bud (Chittenden 1895, Tuttle 1956). Adults may be found on horsenettle through the end of the flowering season, and they will occasionally feed on developing fruits. In the field experiment, potato bud weevils destroyed nearly a third of horsenettle’s entire flower crop and almost 1% of the fruits. The potato bud weevil is common in cultivated potatoes as well, but because it is not considered a pest species, it has not been studied nearly as much as many other potato-feeding insects (Burke 1976, Chittenden 1895). It seems unlikely that destruction of flower buds will negatively affect potato plants’ growth, survival, or tuber production. In a separate controlled study, horsenettle plants subjected to heavy herbivory by bud weevils had significantly greater underground growth than those protected from floral herbivory (Wise and Cummins 2006). If the loss of flowers has the same effect on underground growth in potatoes, potato bud weevils may actually benefit tuber production. A close relative of the potato bud weevil, Anthonomus eugenii Cano (pepper weevil), feeds on Capsicum (pepper) crops in the southern US from 514 Southeastern Naturalist Vol. 6, No. 3 Florida to California as well as in Hawaii (Berdegue et al. 1994, Capinera 2005). The pepper weevil has also been reported to damage flowers and immature fruits of horsenettle in Florida (Aguilar and Servín 2000, Capinera 2005). These weevils do not diapause and thus they need a continuous source of food throughout the year (Capinera 2005). Because their host plants are not available in the winter in Virginia, it is not surprising that I did not encounter pepper weevils in my study. Thrips. Several species of thrips were collected from flowers of horsenettle over the course of this study, including several common crop pests: Thrips tabaci (onion thrips), Frankliniella fusca (tobacco thrips), and F. tritici and F. occidentalis (eastern and western flower thrips). These thrips fed on anthers, causing brown spots and premature wilting. Their damage does not appear to be extreme, but it is possible that they affect pollen production, survival, or removal by pollinators. Meadow voles. Voles were the only non-insect herbivores of horsenettle observed in this study. Voles are generalist herbivores, but horsenettle does not appear to be a preferred food item (Burt and Grossenheider 1980, Pascarella and Gaines 1991). In the field experiment, voles sometimes cut down entire horsenettle ramets if they happened to be transplanted in the voles’ runways. Voles also killed a large number of horsenettle flowers and immature fruits. However, this damage often seemed incidental, as the voles tended not to eat the flowers or fruits they cut down. They were more likely to just gnaw on the cortex of the racemes’ peduncles and fruit pedicels and leave the fruits or flowers dangling on the plant or lying beneath the plant. In the fall and winter, however, meadow voles do consume horsenettle fruits and may cache and disperse their seeds (M.A. Bowers, University of Virginia, Charlottesville, VA, pers. comm.). Fruit-feeding herbivores Pepper maggot. Adults of the tephritid fly Zonosemata electa (pepper maggot) appear in horsenettle populations in July when the first fruits are maturing. Females inject eggs into the fruits, and larvae feed on the pulp. Larvae emerge from fruits in late summer or early fall to pupate in the soil. Many eggs may be laid per fruit, and I have found over twenty immature larvae inside a single fruit. This oviposition behavior differs from Foott’s (1968) observations in Ontario, in which generally only 1 egg, but occasionally up to 3 eggs, were laid per fruit. Out of the many hundreds of pepper maggots I reared from horsenettle fruits over the course of my studies, I almost never observed more than one larva emerge from a fruit. Therefore, larval cannibalism is likely quite common. Successful parasitism, in contrast, was extremely rare. The only evidence of a parasitoid was a single wasp of the genus Diachasmimorpha (Braconidae) that emerged from a pepper maggot puparium. Pepper maggots feed on placentas of fruits and do not appear to affect the seeds, although infestation despoils the pulp. Infested fruits often ooze through oviposition holes when ripening, and they turn black and harden in the fall, while uninfested fruits are yellow and smooth. If the rotten fruits are 2007 M.J. Wise 515 less appealing to fruit-feeding mammals and birds, then pepper maggots may have a detrimental effect on horsenettle seed dispersal. The effect of pepper maggot infestation on fruit and seed dispersal is worth further study. Stem-feeding herbivores Potato stalk borer. Adult Trichobaris trinotata (potato stalk borers) emerge from previous-year stems in the spring, and females deposit an egg in a slit chewed in the axil of a terminal leaf of a young horsenettle ramet. The larva hatches and spends the entire summer feeding on stem pith, eventually pupating at the junction of the stem and root in a nest constructed of fibrous stem shavings (Somes 1916). Adults usually eclose in less than 2 weeks but remain in the stems throughout the winter (Cuda and Burke 1986, Faville and Parrott 1899). None of 960 stems in the field experiment contained more than 1 stalk borer, but I have previously found 2 adults inside larger horsenettle ramets, with 1 at the base of the stem and 1 much higher up. Almost three-fourths of the horsenettle stems in the field experiment exhibited signs of damage by the potato stalk borer. However, only 57% of the stems contained live borers upon dissection. Some of the larvae died of unidentified causes, but many were parasitized by Neocatolaccus tylodermae (Ashmead) (Hymenoptera: Pteromalidae) and a species of Heterospilus (Hymenoptera: Braconidae). Although the potato stalk borer is one of the most destructive pests of cultivated potatoes (Cuda and Burke 1986, Faville and Parrott 1899), horsenettle appears to tolerate its presence very well. In a controlled study, infestation by potato stalk borers had no effect on any horsenettle growth or reproductive measures (M.J. Wise, unpubl. data). In the field study reported here, infested plants produced more seeds on average than those without stalk borers (Wise 2003). This apparent fitness benefit may have been an artifact of the weevils preferentially ovipositing in larger, more vigorous horsenettle plants. Gall midge. Stem galls of cecidomyiid flies were regularly found in some populations over the course of this study, but they were never common, and single ramets rarely contained more than one or two galls. These galls consist of small swellings on the main stem, lateral stems, or on racemes between fruits. Only 4 of the 960 plants in the transplant experiment were galled. All of the individuals I have reared from these galls were Lasioptera solani, though a species of Neolasioptera is reported to be more common in horsenettle (Gagné 1989). Rearing of these gall midges proved difficult because the vast majority of galls were parasitized by proctotrupoid wasps. The small size of the galls and low densities of these gall midges suggest that they are likely to have relatively little impact on horsenettle. Root-feeding herbivores Riley’s clearwing. Besides larvae of the eggplant flea beetle, the only other common root-feeding herbivores were larvae of the moth Synanthedon 516 Southeastern Naturalist Vol. 6, No. 3 rileyana (Riley’s clearwing). The adults, which mimic yellow-jackets, are found on the wing in late summer in northern Virginia. It has been reported that females oviposit on horsenettle stems and leaves, and larvae bore through the stem and downward into the root, eventually pupating in the soil (Somes 1916, Williams et al. 1999). This information is somewhat suspect, however, as the author who reported that adults emerge in August and September also reported that third instar larvae were found in stems in May (Somes 1916). Because horsenettle stems do not survive the winter, it is not clear how the larvae could be present in living stems earlier in the season than the emergence of adults. In my studies, I have found no evidence of insects other than potato stalk borers and their parasitoids in the stems of horsenettle. All of the Riley’s clearwing larvae I have seen were feeding on taproots or thick lateral roots. They appear to bore into the root from the outside and feed close to the cortex, rather than tunneling into roots down through the interior of the stem. Thus, it is likely that females oviposit at the base of horsenettle stems rather than on leaves. I have found clearwing larvae at different stages of development feeding on roots both in the fall and early spring, indicating that the overwintering stage is the larva, and that larval development may not conclude until spring. Summary Over seven years of observations in northern Virginia, I recorded 32 species of herbivores that regularly fed upon the leaves, flowers, fruits, stems, or roots of horsenettle. Of these, 11 species consistently caused considerable damage in at least some horsenettle populations. The false potato beetle was the most conspicuous herbivore, damaging large numbers of leaves, flowers, and fruits. The other main folivores were the eggplant flea beetle, eggplant leafminer, eggplant tortoise beetle, eggplant lace bug, and citrus gall midge, in general order of abundance. The potato bud weevil, the pepper maggot, and the potato stalk borer were consistently the most damaging herbivores of flowers, fruits, and stems, respectively. The moth Frumenta nundinella damaged leaves, meristems, and flowers. The only non-insect herbivore, the meadow vole, destroyed large numbers of flowers and fruits in some populations. Acknowledgments The University of Virginia’s Blandy Experimental Farm provided logistical and financial support throughout the 7 years of this research via graduate research fellowships, field station grants from the National Science Foundation (NSF-BIR- 9512202) to M.A. Bowers and E.F. Connor, and an REU site grant (NSF-DBI-9912164) to M.A. Bowers and D.E. Carr. This work was also supported by an NSF Dissertation Improvement Grant (NSF-DEB-00-73176) to M.D. Rausher and M.J. Wise, a US EPA STAR Fellowship (U-915654-01-0) to M.J. Wise, and NSF grant (DEB-0515483) to W.G. Abrahamson and M.J. Wise. Any opinions, findings, and conclusions expressed in this material are those of the author and do not 2007 M.J. Wise 517 necessarily reflect the views of the US Environmental Protection Agency or the National Science Foundation. I thank J.A. Leachman and J. Byrd for providing invaluable assistance in the field study of 2001. Thanks also to W.G. Abrahamson, C.P. Blair, N. Dorchin, P.J. 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Ecological Entomology 27:115–122. 2007 M.J. Wise 521 Appendix 1.Taxonomy, feeding location, and host range of insect herbivores of horsenettle observed in northern Virginia from 1996–2002. The common names are from the Entomological Society of America (2007). For species without common names, the common name of the family or order is shown in parentheses. The plant organs are: Lf = leaf, St = stem, Fl = flower, Fr = fruit, and Rt = root. The host ranges are: monophagous = specialist on horsenettle; oligophagous = restricted largely to species in family Solanaceae; polyphagous = feeds on a large number of species, including non-solanaceous plants; and ? = unknown. Plant organs Order, Family Species Common name fed upon Host range Hemiptera Tingidae Gargaphia solani Heidemann Eggplant lace bug Lf Oligophagous Homoptera Membracidae Entylia bactriana Germar (Treehopper) Lf Polyphagous Cercopidae Philaenus spumarius (Linnaeus) Meadow spittlebug Lf, St Polyphagous Cicadellidae Draeculacephala antica (Walker) (Leafhopper) Lf Polyphagous Flatidae Ormenis sp. (Planthopper) Lf ? Acanaloniidae Acanalonia bivittata (Say) (Planthopper) Lf Polyphagous Aleyrodidae Trialeurodes abutilonea (Haldeman) Bandedwinged whitefly Lf Polyphagous T. vaporariorum (Westwood) Greenhouse whitefly Lf Polyphagous Aphidae Unidentified (Aphid) Lf, St ? Thysanoptera Thripidae Frankliniella fusca (Hinds) Tobacco thrips Fl Polyphagous F. occidentalis (Pergande) Western flower thrips Fl Polyphagous F. tritici (Fitch) Flower thrips Fl Polyphagous Thrips tabaci Lindeman Onion thrips Fl Polyphagous 522 Southeastern Naturalist Vol. 6, No. 3 Plant organs Order, Family Species Common name fed upon Host range Coleoptera Meloidae Epicauta pestifera Werner Margined blister beetle Lf, Fl Polyphagous Chrysomelidae Leptinotarsa juncta (Germar) False potato beetle Lf, Fl, Fr Monophagous L. decemlineata (Say) Colorado potato beetle Lf, Fl, Fr Oligophagous Epitrix fuscula Crotch Eggplant flea beetle Rt, Lf Oligophagous Gratiana pallidula (Boheman) Eggplant tortoise beetle Lf Oligophagous Curculionidae Anthonomus nigrinus Boheman Potato bud weevil Fl Oligophagous Trichobaris trinotata (Say) Potato stalk borer St Oligophagous Diptera Cecidomyiidae Prodiplosis longifila Gagné Citrus gall midge Lf Polyphagous Lasioptera solani Felt (Gall midge) St Monophagous Tephritidae Zonosemata electa (Say) Pepper maggot Fr Oligophagous Lepidoptera Gelechiidae Tildenia inconspicuella (Murtfeldt) Eggplant leafminer Lf Oligophagous Frumenta nundinella (Zeller) (Moth) St, Fl, Fr Monophagous Sesiidae Synanthedon rileyana (H. Edwards) Riley’s clearwing moth Rt Oligophagous Tortricidae Argyrotaenia velutinana (Walker) Redbanded leafroller Lf Polyphagous Platynota flavedana (Clemens) (Moth) Lf Polyphagous Sparganothis sulfureana (Clemens) Sparganothis fruitworm Lf Polyphagous Sphingidae Manduca sexta (Linnaeus) Tobacco hornworm Lf, Fl, Fr Oligophagous Arctiidae Estigmene acrea (Drury) Salt marsh caterpillar Lf, Fl Polyphagous