Iain D. Paterson

Two in one: cryptic species discovered in biological control agent populations using molecular data and crossbreeding experiments

Abstract There are many examples of cryptic species that have been identified through DNA‐barcoding or other genetic techniques. There are, however, very few confirmations of cryptic species being reproductively isolated. This study presents one of the few cases of cryptic species that has been confirmed to be reproductively isolated and therefore true species according to the biological species concept. The cryptic species are of special interest because they were discovered within biological control agent populations. Two geographically isolated populations of Eccritotarsus catarinensis (Carvalho) [Hemiptera: Miridae], a biological control agent for the invasive aquatic macrophyte, water hyacinth, Eichhornia crassipes (Mart.) Solms [Pontederiaceae], in South Africa, were sampled from the native range of the species in South America. Morphological characteristics indicated that both populations were the same species according to the current taxonomy, but subsequent DNA analysis and breeding experiments revealed that the two populations are reproductively isolated. Crossbreeding experiments resulted in very few hybrid offspring when individuals were forced to interbreed with individuals of the other population, and no hybrid offspring were recorded when a choice of mate from either population was offered. The data indicate that the two populations are cryptic species that are reproductively incompatible. Subtle but reliable diagnostic characteristics were then identified to distinguish between the two species which would have been considered intraspecific variation without the data from the genetics and interbreeding experiments. These findings suggest that all consignments of biological control agents from allopatric populations should be screened for cryptic species using genetic techniques and that the importation of multiple consignments of the same species for biological control should be conducted with caution.

The Herbivorous Arthropods Associated with the Invasive Alien Plant, Arundo donax, and the Native Analogous Plant, Phragmites australis, in the Free State Province, South Africa

The Enemy Release Hypothesis (ERH) predicts that when plant species are introduced outside their native range there is a release from natural enemies resulting in the plants becoming problematic invasive alien species (Lake & Leishman 2004; Puliafico et al. 2008). The release from natural enemies may benefit alien plants more than simply reducing herbivory because, according to the Evolution of Increased Competitive Ability (EICA) hypothesis, without pressure from herbivores more resources that were previously allocated to defence can be allocated to reproduction (Blossey & Notzold 1995). Alien invasive plants are therefore expected to have simpler herbivore communities with fewer specialist herbivores (Frenzel & Brandl 2003; Heleno et al. 2008; Heger & Jeschke 2014).

Encompassing the relative non-target risks from agents and their alien plant targets in biological control assessments

Criticisms about the safety of biological control of alien plants has resulted in a risk-averse approach, where the risks posed by the agent are paramount and the risks posed by the alien plant are neglected. We argue that the risk associated with non-target damage from agents needs to be assessed relative to that of their target alien plants. A literature review of the non-target risks associated with biological control agents was undertaken in terms of the risk to native species from agents relative to the risk to native species from their alien plant targets. We then developed a framework that compares the consequence with the likelihood of non-target damage for both agents and their targets to provide an overall risk rating. Assessments of the risk of damage from both agents and their target alien plants will enable researchers, managers and policy makers to better assess the risks from biological control.

Prioritisation of potential agents for the biological control of the invasive alien weed, Pereskia aculeata (Cactaceae), in South Africa.

Pereskia aculeata Miller (Cactaceae) is an invasive alien species in South Africa that is native in Central and South America. In South Africa, P. aculeata outcompetes native plant species leading to a reduction in biodiversity at infested sites. Herbicidal and mechanical control of the plant is ineffective and unsustainable, so biological control is considered the only potential solution. Climatic matching and genotype matching indicated that the most appropriate regions in which to collect biological control agents were Santa Catarina and Rio de Janeiro provinces in Southern Brazil. Surveys throughout the native distribution resulted in 15 natural enemy species that were associated with the plant. Field host range data, as well as previous host plant records, were used to prioritise which of the species were most likely to be suitably host specific for release in South Africa. The mode of damage was used to determine which species were most likely to be damaging and effective if released. The most promising species prioritised for further study, including host specificity and impact studies, were the stem-wilter Catorhintha schaffneri Brailovsky & Garcia (Coreidae); the stem boring species Acanthodoxus machacalis Martins & Monné (Cerambycidae), Cryptorhynchus sp. (Curculionidae) and Maracayia chlorisalis (Walker) (Crambidae) and the fruit galler Asphondylia sp. (Cecidomyiidae). By prioritising the potential biological control agents that are most likely to be host-specific and damaging, the risk of conducting host specificity testing on unsuitable or ineffective biological control agents is reduced.

The effect of host plant intraspecific genetic variation on the fitness of a monophagous biological control agent

Abstract Variation in insect life-history traits when developing on different host plant genotypes with known genetic relationships was tested using the monophagous biological control agent Phenrica guérini Bechyné (Chrysomelidae) and its host plant, Pereskia aculeata Miller (Cactaceae). Differences in insect fitness among tested host plant genotypes were expected because of geographic isolation and large genetic distances between plant genotypes, and because P. guérini has been associated with some of the plant accessions in the field while others have never been exposed to herbivory by the insect. There was little variation in insect life-history traits among plant genotypes and no differences in the insects ability to utilise different plant genotypes. The results of the study suggest that, in some cases, biological control agents collected from the native genotype most closely related to the target weed population will not always be more effective than those collected from more distantly related genotypes.

Expansive reed populations—alien invasion or disturbed wetlands?

In southern Africa a pattern of Phragmites spp. reed expansion has occurred in recent decades that has shown a similar trend to cryptic invasions reported in North and South America. This study used molecular techniques to explore the phylogeography of P. australis and P. mauritianus and found no evidence of cryptic invasion. The expansion of P. australis and P. mauritianus is therefore occurring within native haplotypes and is most likely a result of anthropogenic activity that has disturbed wetlands.

Exploring the Origin and Genetic Diversity of the Giant Reed, Arundo donax in South Africa

The giant reed, Arundo donax is one of the worst invasive alien species globally, including South Africa, where it invades riparian areas across the country. Biological control is being considered to address the invasive potential and negative impacts of the weed. This study investigated the phylogeography of A. donax to guide the biological control program. To determine plant haplotype and genetic diversity, three regions of the chloroplast were sequenced and three microsatellite markers were analyzed in 40 samples from across the plants distribution in South Africa. It was determined that all populations of A. donax in South Africa were haplotype M1, which is the most widely distributed haplotype worldwide, believed to originate from the Indus Valley, Asia. In addition, no genetic diversity was found, indicating that all the A. donax populations in South Africa are essentially one clone. The results indicate that suitable biological control agents are likely to be found in the ancient native range of haplotype M1. This research has contributed to the global understanding of the phylogeography of A. donax and will guide the biological control program in South Africa. Nomenclature: Giant reed; Arundo donax L. ABKDO.

Predicting the risk of non-target damage to a close relative of a target weed using sequential no-choice tests, paired-choice tests and olfactory discrimination experiments

ABSTRACT We investigated host-plant utilisation by the candidate biocontrol agent Paradibolia coerulea (Coleoptera: Chrysomelidae) on the target plant Spathodea campanulata Beauv. (Bignoniaceae) and a closely related non-target plant, Kigelia africana (Lam.) Benth. (Bignoniaceae). Paired-choice and sequential no-choice experiments were performed and coupled with olfactory discrimination experiments to test the insects’ responses to volatiles from both plant species as well as to cues from conspecific beetles. Although K. africana was utilised by P. coerulea, S. campanulata was preferred for both adult feeding and oviposition. Interestingly, whereas females were attracted to olfactory cues emitted by S. campanulata, males demonstrated no such olfactory discrimination. Females were also attracted to cues deposited by males, and males were deterred by cues from other males, but neither sex responded to female olfactory cues. Very few eggs were recorded on K. africana and none of the larvae that hatched on K. africana survived the first instar. Both S. campanulata and K. africana are suitable for adult feeding, but persistent utilisation of K. africana in the field is unlikely because larval development is only possible on S. campanulata and because the adult females are strongly attracted to volatiles emitted by the target plant. Nevertheless, if P. coerulea is released as a biocontrol agent, spill-over adult feeding could potentially occur on K. africana growing sympatrically with S. campanulata. Because P. coerulea cannot complete its development on K. africana, non-target damage will only occur where the target plant is present, with an intensity dependent on densities of adult beetles locally.

Effect of water trophic level on the impact of the water hyacinth moth Niphograpta albiguttalis on Eichhornia crassipes.

Eutrophication contributes to the proliferation of alien invasive weed species such as water hyacinth Eichhornia crassipes. Although the South American moth Niphograpta albiguttalis was released in South Africa in 1990 as a biological control agent against water hyacinth, no post-release evaluations have yet been conducted here. The impact of N. albiguttalis on water hyacinth growth was quantified under low-, medium- and high-nutrient concentrations in a greenhouse experiment. Niphograpta albiguttalis was damaging to water hyacinth in all three nutrient treatments, but significant damage in most plant parameters was found only under high-nutrient treatments. However, E. crassipes plants grown in high-nutrient water were healthier, and presumably had higher fitness, than plants not exposed to herbivory at lower-nutrient levels. Niphograpta albiguttalis is likely to be most damaging to water hyacinth in eutrophic water systems, but the damage will not result in acceptable levels of control because of the plants high productivity under these conditions. Niphograpta albiguttalis is a suitable agent for controlling water hyacinth infestations in eutrophic water systems, but should be used in combination with other biological control agents and included in an integrated management plan also involving herbicidal control and water quality management.

Evaluating the efficacy of Hypogeococcus sp. as a biological control agent of the cactaceous weed Cereus jamacaru in South Africa

We evaluated the efficacy of Hypogeococcus sp. (Hemiptera: Pseudococcidae) as a biological control agent of the cactaceous weed Cereus jamacaru De Candolle (Queen of the Night cactus) in South Africa. This weed has been described as being under complete biological control due to the action of Hypogeococcus sp., although no formal post-release evaluation had been conducted prior to this study. Biological control was associated with significant reductions in fruiting, plant survival and plant densities, while plant population age structures were negatively affected. Weed populations infected by Hypogeococcus sp. were typified by low or non-existent recruitment and are expected to diminish with time. Populations where Hypogeococcus sp. was absent displayed extensive recruitment, and are predicted to expand or self-replace, if left unchecked. These data indicate that Hypogeococcus sp. has a significant negative effect on C. jamacaru at the individual plant and population level, and given sufficient time provides complete biological control over this weed in South Africa.