RESEARCH ARTICLE

 

Natural enemy release or biotic resistance? Insect herbivores associated with the exotic Solanum viarum (Solanaceae) and a sympatric native congener in KwaZulu-Natal, South Africa

 

 

Terence Olckers; Kwanele Msele; Daniella Egli

School of Life Sciences, University of KwaZulu-Natal, Scottsville, South Africa

Correspondence

 

 

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ABSTRACT

Native to South America, Solanum viarum Dunal (tropical soda apple; Solanaceae) is naturalised in several countries globally. The plant is a major invader in the southern USA, but has minor weed status in South Africa. We investigated whether S. viarum has escaped natural enemy pressure or has recruited insect herbivores from the local Solanum flora, which are exerting some level of biotic resistance. Insect species richness and abundance and the resulting levels of herbivory were compared between plants from sympatric populations of S. viarum and the native Solanum dasyphyllum Schumacher and Thonning in the KwaZulu-Natal Midlands. Foliage, floral material, and fruits were collected across seasons from 20 plants of each species and assessed in the laboratory. Despite no significant differences between the two species in the size of the sampled plants, S. viarum displayed significantly lower insect herbivore diversity and abundance and suffered significantly lower levels of damage to its photosynthetic and reproductive tissues. Five of the 11 specialist herbivore species recorded on S. dasyphyllum were associated with S. viarum, but in substantially lower numbers and in fewer samples. The flowerbud-galling moth Scrobipalpa sp. (Gelechiidae), which prevents fruiting in S. dasyphyllum, was absent on S. viarum and indicative of the negligible floral damage on S. viarum. Although the fruit of S. viarum were occasionally utilised by specialist herbivores, seed damage was similarly negligible. Due to its release from specialist natural enemies and with no evidence of biotic resistance, S. viarum may increase in weed status in South Africa.

Keywords: insect herbivore recruitment; invasive Solanaceae; Solanum dasyphyllum; tropical soda apple; weed ecology

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INTRODUCTION

Solanum viarum Dunal (Solanaceae), commonly known as tropical soda apple, is a prickly shrub that is native to northern Argentina, southern Brazil, Uruguay and Paraguay (Mullahey et al. 1993; Olckers et al. 2002; Welman 2003). The plant is naturalised in several countries including Australia, China, India, Mexico, the United States of America, the West Indies, and South Africa (Coile 1993; Welman 2003; Diaz et al. 2014). Solanum viarum bears broad sticky leaves due to glandular trichomes, numerous thorns, distinctive yellow fruits, and cream-coloured flowers (Coile 1993; Mullahey et al. 1993). Individual plants can produce in excess of 50 000 seeds annually, which are dispersed by cattle, wild animals, contaminated agricultural produce and machinery, and humans (Coile 1993; Mullahey et al. 1993). The unpalatability of its foliage for browsing animals contributes largely to the plant's competitive advantage (Mullahey et al. 1993). Solanum viarum became a major invasive weed of pastures, conservation areas and disturbed habitats in the southern states of the USA, leading to the implementation of a successful biological control programme (Diaz et al. 2014).

The Enemy Release Hypothesis (Keane and Crawley 2002) proposes that invasive exotic plants gain a competitive advantage over native flora, due to escape from their co-evolved natural enemies outside of their natural habitats. This phenomenon can interact with other factors, including resource availability, lack of biotic resistance, and disturbance, to enhance the success of invasion by exotic plants in their new habitats (Blumenthal 2006; Maron and Vilá 2001; Jeschke 2014). Although widely distributed in the Eastern Cape and KwaZulu-Natal provinces of South Africa, and neighbouring Swaziland (Welman 2003), S. viarum is currently regarded as a weed of minor importance (Welman 2003; Henderson 2020). One possible explanation for the plant's low weed status in South Africa is that it has attracted specialist insect herbivores from native plants in the genus Solanum (Olckers and Hulley 1989a, b, 1991) and/or generalist herbivores, thereby substituting for natural enemy release and subjecting it to some degree of natural control. This scenario would conform to the Biotic Resistance Hypothesis (see Maron and Vilá 2001; Jeschke 2014).

The aim of this study was to determine whether S. viarum has recruited specialist insect herbivores from related congeneric plants or has remained relatively free of insect attack. This was achieved by comparing the insect herbivore faunas and the levels of damage inflicted on the foliage, flowers and fruit of S. viarum versus the native congener Solanum dasyphyllum Schumacher and Thonning (previously called S. cf. acanthoideum E. Meyer in Olckers and Hulley (1991)). These two species are similar in size and architecture and typically co-occur in the same habitats in the Midlands region of KwaZulu-Natal, where S. viarum was first recorded (Welman 2003). Low insect herbivore species richness and abundance, compounded by a lack of specialist species, and consequently low levels of damage on S. viarum relative to S. dasyphyllum would indicate natural enemy release (e.g. DeWalt et al. 2004). In contrast, equivalent insect herbivore faunas and levels of damage on the two Solanum species would indicate biotic resistance through natural enemy substitution and explain the limited invasiveness of S. viarum recorded at present.

 

MATERIALS AND METHODS

Study sites

Individual plants of S. viarum and S. dasyphyllum were sampled at six localities around Pietermaritzburg, KwaZulu-Natal province, South Africa where populations of both species occur in sympatry (Table 1). Twenty plants of each species were sampled on nine occasions during 2023/24. Voucher specimens of both species were lodged in the University of KwaZulu-Natal John Bews Herbarium (NU).

Sampling protocol

On each sampling occasion, equal numbers of plants of both species were sampled, with various components (foliage, fruits, and flowers) collected for later analysis. The height of each plant was measured prior to sampling. A branch that included the top 30 cm of foliage was removed from each plant, placed in a paper bag, and stored in a freezer for later assessment. When present, additional floral tissues (flowers and buds) and fruit were collected from each plant and placed in emergence containers in the laboratory to rear immature insect stages to adulthood. The leaves from the frozen material were inspected under a dissecting microscope to record ectophagous insects, while the stems, fruits, and floral material were dissected to record endophagous immature stages. Floral and fruit material in the emergence containers were dissected after 2-3 weeks and 6-8 weeks, respectively, to record any remaining immature stages.

All collected insects, including herbivores, predators and parasitoids, were preserved in 70% alcohol or pinned for later comparisons and the numbers of individuals of each insect species were recorded for each sampled plant. Species where single individuals were recorded only once were excluded. Specialist herbivore taxa were regarded as those typically associated with native Solanum species in South Africa (see Olckers and Hulley 1989a, b, 1991; Olckers et al. 1995).

Assessments of insect damage were made during the processing of the different plant tissues. Leaf damage on each sampled plant was scored on a scale from 0 to 3, which ranged from no clear damage (0), very little damage (1), moderate damage (2) to considerable damage (3). Floral and fruit damage for each sampled plant was recorded as the percentages of flowerbuds/ flowers and fruit (from both the frozen samples and emergence containers) that were infested by insects.

Statistical analysis

The data were analysed using IBM SPSS version 29. Since the data did not meet the assumptions of normality or equality of variances, non-parametric tests and generalised linear models were used to determine statistical significance (p < 0.05). Plant height, insect species richness, insect abundance, and leaf damage scores were compared between the two Solanum species using independent-samples median tests (Yates's continuity corrected). The proportions of insect-infested versus uninfested floral material and fruit were compared between the two plant species using models that incorporated a binomial distribution and a logit-link function. These models were corrected for over-dispersion by means of scale weight variables and significance (p < 0.05) was determined using Wald chi-square statistics.

 

RESULTS

Insect species richness and abundance

Nineteen insect species (15 herbivorous) were recorded on S. viarum, compared to 33 species (26 herbivorous) on S. dasyphyllum. Consequently, there was significantly lower median insect species richness, which included all recorded species (χ² = 5.385, df = 1, p = 0.02) and herbivorous species (χ² = 14.731, df = 1, p < 0.001) on S. viarum (Figure 1). Similarly, there was significantly lower median insect abundance on S. viarum in relation to all recorded insects (χ² = 10.025, df = 1, p = 0.002) and herbivorous insects (χ² = 16.900, df = 1, p < 0.001) (Figure 2). There was no significant difference in median plant height between S. viarum and S. dasyphyllum (χ² = 0.100, df = 1, p = 0.752), suggesting that plant size did not influence insect species richness or abundance.

 

 

 

 

Insect herbivore composition

The insect herbivore fauna associated with S. viarum was largely comprised of generalist species that were present in a low proportion of samples. Only five species, which included one foliage feeder, one flower feeder and three fruit feeders, were regarded as specialists that are typically associated with native Solanum species, but none were recorded in more than 30% of the samples (Table 2). In contrast, the insect herbivore fauna associated with S. dasyphyllum included 11 specialists, comprising four foliage feeders, two flower feeders and five fruit feeders, with seven species recorded in more than 30% of the samples (Table 2). When present on both species, the incidence (i.e. presence in samples) and mean abundance of these specialist species was substantially higher on S. dasyphyllum (Table 2).

Levels of insect damage

On average, very low leaf damage scores (mean ± SE = 1.0 ± 0.1) were recorded on S. viarum and were significantly lower (χ² = 22.727, df = 1, p < 0.001) than the moderate scores (2.3 ± 0.2) recorded on S. dasyphyllum. Most leaf damage on S. dasyphyllum was attributed to adults and larvae of the herbivorous ladybird Epilachna hirta (Coccinellidae) and adults of the flea beetle Chaetocnema sp. (Chrysomelidae), which were recorded in >50% of foliar samples (Table 2).

The percentage of floral material infested by endophagous insects (Figure 3) was also significantly lower (χ² = 12.218, df = 1, p < 0.001) on S. viarum (mean ± SE = 3.0 ± 1.7%) than on S. dasyphyllum (48.1 ± 8.7%). The flower-boring beetle Pria sp. (Nitidulidae) was recorded on both species, albeit less frequently and abundantly on S. viarum (Table 2). In contrast, the flower-galling moth Scrobipalpa sp. (Gelechiidae), which prevents fruit formation by S. dasyphyllum, was absent on S. viarum but present in 78% of floral samples collected from S. dasyphyllum (Table 2). On average, 41.6% (± 9.3%) of the floral components sampled on S. dasyphyllum plants comprised galled buds, accounting for the major difference in floral damage between the two Solanum species.

 

 

Similarly, the percentage of fruit infested by endophagous insects (Figure 3) was significantly lower (χ² = 9.708, df = 1, p = 0.002) on S. viarum (mean ± SE = 11.5 ± 4.1%) than on S. dasyphyllum (49.2 ± 9.0%). Although the fruit-boring moth D. laisalis (Pyraustidae) and two fruit-feeding flies, S. ophyroides (Lonchaeidae) and an unidentified species of Agromyzidae, were recorded on both Solanum species, they were more frequent and abundant on S. dasyphyllum (Table 2). In any event, the impact of these fruit borers was negligible, with D. laisalis caterpillars damaging few seeds within infested fruits.

 

DISCUSSION

Solanum viarum has been present in South Africa for more than 60 years, with the first recorded specimen collected around Pietermaritzburg, KwaZulu-Natal in 1962 (Welman 2003).

However, the plant was not recognised by Arnold and De Wet (1993) in their list of Solanaceae present in South Africa and its identity was only confirmed later (see Welman 2003). The plant has previously been misidentified and confused with both exotic (e.g. S. aculeatissimum Jacquin) and native (e.g. S. acanthoideum E. Meyer and S. panduriforme E. Meyer) congeners in South Africa (Olckers et al. 1995; Hill et al. 1997; Welman 2003). In South Africa, S. viarum has low weed status (Welman 2003) relative to other exotic congeners, notably S. elaeagnifolium Cavanilles, S. mauritianum Scopoli and S. sisymbriifolium Lamarck, and is currently not listed under the South African alien plant legislation (Henderson 2020). Since the plant has been brought under biological control in the USA, following the introduction of the tortoise beetle Gratiana boliviana Spaeth (Chrysomelidae), we considered whether recruited native specialists were having a similar impact in South Africa. In particular, the insect faunas of native Solanum species are largely comprised of oligophagous species that utilise several congeneric host-plant species (see Olckers and Hulley 1989a, b, 1991, 1995; Olckers et al. 1995) and could thus have included S. viarum in their host range.

However, our study revealed that S. viarum has remained largely free of natural enemy pressure, with significantly lower insect herbivore richness, abundance, specialist composition, and damage levels relative to the native S. dasyphyllum. These trends were previously reported in South Africa for the exotic S. elaeagnifolium (Hill et al. 1993; Olckers and Hulley 1995), S. mauritianum (Olckers and Hulley 1989a, 1991, 1995) and S. sisymbriifolium (Hill et al. 1993; Olckers and Hulley 1995). Although S. viarum and S. dasyphyllum belong to the subgenus Leptostemonum Bitter, S. viarum falls under the Section Acanthophora Dunal, which is not native to southern Africa (Welman 2003; Vorontsova et al. 2013). In addition, Hill et al. (1997) reported two types of glandular trichomes on the leaves of S. viarum (misidentified as S. acanthoideum), which are renowned as anti-herbivore defences and are not typical of S. dasyphyllum leaves. Indeed, glandular trichomes on the leaves of S. sisymbriifolium significantly reduced the feeding and survival of the native Solanum-feeding tortoise beetle Conchyloctenia tigrina Olivier (Chrysomelidae), but not the South American tortoise beetle Gratiana spadicea (Klug) that utilises this plant as a host, thereby explaining the poor insect herbivore fauna associated with the plant in South Africa (Hill et al. 1993).

Beside glandular trichomes, the chemical defences of S. viarum may also prohibit its utilisation by native solanaceous insects. High concentrations of secondary metabolites, notably phenolic compounds and acylsugars, together with leaf trichomes, deterred feeding and survival of the polyphagous agricultural pest Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae), advocating the use of S. viarum as a trap plant in croplands (Gyawali et al. 2022). These considerations, evidenced by the absence of specialists like the flowerbud-galling moth Scrobipalpa sp. that reduces fruiting in several native Solanum species (Olckers and Hulley 1989b, 1991), suggest that S. viarum could increase its weed status in South Africa. In particular, despite the unpalatability of the plant's foliage, its ripe yellow fruit are ingested by cattle and wild animals, which facilitated its rapid distribution in the USA (Mullahey et al. 1993; Diaz et al. 2014).

Since S. viarum has a low weed status in South Africa, the Enemy Release Hypothesis (Keane and Crawley 2002), which predicts the opposite, does not explain the plant's population status. Rather, S. viarum is a minor weed despite exhibiting release from specialist natural enemies. However, we acknowledge that the study did not consider the role of plant pathogens as specialist natural enemies in this context. Although there are several examples of biotic resistance, where exotic plants have recruited diverse assemblages of native herbivores that have reduced their invasive properties (Maron and Vilá 2001), this study produced no evidence for the Biotic Resistance Hypothesis (Jeschke 2014).

While other biotic factors may be limiting its invasion potential (e.g. resistance from native flora), S. viarum may still be in the early stages of invasion and increase its weed status in the future. Should this occur, biological control using the defoliating beetle G. boliviana (Diaz et al. 2014) should be considered, since neither native solanaceous specialists nor generalist species are contributing to the plant's control.

 

ACKNOWLEDGEMENTS

This study involved a continuation of the BSc (Hons) research project of the second author, which was funded by the School of Life Sciences, University of KwaZulu-Natal. The manuscript was improved following the comments of two anonymous reviewers.

 

AUTHOR CONTRIBUTIONS

TO: conceptualisation; project administration; investigation; data curation; formal analysis; supervision; writing - original draft.

KM: investigation; data curation; formal analysis; writing -review and editing.

DE: investigation; supervision; writing - review and editing.

 

ORCID IDS

Terence Olckers: https://orcid.org/0000-0001-6750-8683

Kwanele Msele: https://orcid.org/0000-0003-2030-8224

Daniella Egli: https://orcid.org/0000-0002-6922-7970

 

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Correspondence:
Terence Olckers
Email: Olckerst@ukzn.ac.za

Received: 31 July 2024
Accepted: 4 September 2024