Research article: life history and host range of Prochoerodes onustaria,an unsuitable classical biological control agent of Brazilian peppertree

The life history and host range of the South American defoliator Prochoerodes onustaria (Lepidoptera: Geometridae) were examined to determine its suitability as a classical biological control agent of the invasive weed Brazilian Peppertree, Schinus terebinthifolia, in the U.S.A. Larvae were collected feeding on S. terebinthifolia in Brazil and were colonised and tested in quarantine. Life history observations indicated that 54% (n?=?63) of larvae reared on S. terebinthifolia leaves survived to adulthood and 65% of adults (n?=?34) required five instars. Development time from eclosion to adult did not differ by sex: males required 42.9?±?1.1 days and females required 41.1?±?0.9 days. No-choice host range tests were conducted on 11 species in two families (Anacardiaceae and Sapindaceae), including U.S.A. native, commercial, and ornamental species. Larvae completed development on all species, although survival differed significantly among them. Larvae fed Anacardium occidentale, Cotinus coggygria, Dodonaea viscosa, and Mangifera indica demonstrated higher survival than those on S. terebinthifolia, whereas survival was reduced among larvae fed Metopium toxiferum and Comocladia dodonaea. Consumption was significantly greater on M. toxiferum than on the other species. The results presented here suggest that P. onustaria is highly polyphagous, feeding and completing development on members of two related plant families, and is not suitable for biological control of Brazilian peppertree in the U.S.A.     

Host range testing and life history of the defoliator Hymenomima nr. memor: an unsuitable biological control agent for Schinus terebinthifolia in the U.S.A.

Host range of larvae of Hymenomima nr. memor (Lepidoptera: Geometridae) was examined in quarantine to evaluate its suitability as a biological control of Brazilian peppertree, Schinus terebinthifolia. Brazilian peppertree, S. terebinthifolia is an environmental and agricultural weed from South America that had invaded many subtropical and tropical areas of the world including Florida and Hawaii, USA. Laboratory life history and quarantine host range studies of H. memor were conducted with no-choice feeding tests. These tests included eight species of the Anacardiaceae and one species of Sapindaceae. Larvae of H. memor had five to six instars with each head capsule width increasing by 1.68-X. Development time from neonate to adult was 46.7?±?2.2 days. In host range tests, neonates completed development to the adult stage on all non-target species, except Toxicodendron radicans. Moreover, developmental times were delayed and pupal weights were reduced for larvae fed Spondias purpurea leaves. Due to the broad host range exhibited by H. memor larvae, this species will not be considered as a biological control agent of S. terebinthifolia in the continental U.S.A.     

Host range of the leaf-tier Tentamen atrivirgulatum Metz (Lepidoptera: Gelechiidae); an unsuitable candidate for biological control of Brazilian peppertree

ABSTRACT

The life history and host range of the South American leaf-tier Tentamen atrivirgulatum Metz, 2019 (Lepidoptera: Gelechiidae) was evaluated to determine its suitability for classical biological control of invasive Brazilian peppertree, Schinus terebinthifolia, in the USA. Larvae were collected during a survey in the native range of Brazil feeding on Brazilian peppertree. A quarantine colony was established and no-choice tests were conducted to determine the host range of this species. The results of these tests indicated that the larvae fed and completed development on seven of the eleven non-target species tested. Percent survival on these non-targets ranged from 20% to 100%. Larval survival was 50% when fed the target weed Brazilian peppertree. When larvae were fed leaves of these non-targets, pupal weights were significantly lower only for those fed Pistacia chinensis. Development time to the pupal and adult stages did not differ with larval diet. These no-choice results indicate T. atrivirgulatum larvae have a broad host range and thus this species will not be developed as a biological control agent for Brazilian peppertree in the USA.     

Native range density,host utilisation and life history of Calophya latiforceps (Hemiptera: Calophyidae): an herbivore of Brazilian Peppertree (Schinus terebinthifolia)

Native range and life history studies of an agent provide critical information during the early stages of a weed biological control programme. Brazilian peppertree is considered to be one of the worst invasive trees of Florida uplands because of negative environmental impacts and lack of effective long-term control methods. A potential biological control agent of Brazilian peppertree, Calophya latiforceps Burckhardt (Hemiptera: Calophyidae), was recently discovered in the state of Bahia, Brazil. Leaf feeding by the nymphs of C. latiforceps stimulates the tree to form pit galls. The objectives of this study were to quantify gall densities in Bahia and to study the life history adaptations of C. latiforceps under greenhouse conditions. Densities of galls and their mortality sources were recorded in August 2012 and March 2013 from trees located along linear transects. Gall density per leaf ranged from 1.6 to 37.5 and 0.3 to 12.8, in August and March, respectively. Nymphal mortality due to parasitism and entomopathogens ranged from 1.2 to 13.8%. Greenhouse observations of host colonisation and evaluations of immature survival and adult performance were conducted using plants from Bahia. A critical step for host colonisation was gall initiation in response to nymphal feeding. Herbivory by C. latiforceps resulted in stunted growth, leaf deformation, yellowing and shedding of leaves. Immature survival and development time were influenced by tree, and ranged from 11 to 75% (average 40%), and 35 to 53 days (average 38.6 days), respectively. Adults lived in average for 9.3 ± 0.6 days; and females laid 85.8 ± 16.4 eggs. C. latiforceps appears to have characteristics of a promising candidate for biological control of Brazilian peppertree.     

Role of molecular genetics in identifying ‘fine tuned’ natural enemies of the invasive Brazilian peppertree, <Emphasis Type="Italic">Schinus terebinthifolius</Emphasis>: a review

Brazilian peppertree, Schinus terebinthifolius Raddi (Sapindales: Anacardiaceae), is a highly successful invasive species in the continental United States, Hawaiian archipelago, several Caribbean Islands, Australia, Bermuda, and a number of other countries worldwide. It also is one of only a few invasive intraspecific hybrids that has been well characterized genetically. The natural enemy complex of Brazilian peppertree includes two thrips and two psyllids that appear to be highly adapted to specific haplotypes or their hybrids. Successful biological control of Brazilian peppertree will require careful matching of the appropriate natural enemies with their host plant genotypes. The Brazilian peppertree model reviewed here could provide a useful framework for studying biological control agents on other invasive weed species that have exhibited intraspecific hybridization.     

Galls induced by Calophya latiforceps (Hemiptera: Calophyidae) reduce leaf performance and growth of Brazilian peppertree

Schinus terebinthifolia Raddi (Anacardiaceae) (Brazilian peppertree) is one of the most serious terrestrial invasive plants in Florida. The leaf galling psyllid, Calophya latiforceps Burckhardt (Hemiptera: Calophyidae), was discovered feeding on the Brazilian peppertree in Bahia, Brazil, in 2010, and is being evaluated for release as a biological control agent. In order to understand how this candidate biological control agent affects the growth of S. terebinthifolia, we measured the effect of the psyllid on photosynthesis, leaf chlorophyll content and plant growth. Infested plants had lower photosynthesis compared to uninfested plants 30 and 45 days after gall initiation, and chlorophyll content was lower over a 70-d period. Plant height was reduced 31% and biomass 11% after three months of infestation. Results of these studies suggest that C. latiforceps will negatively affect the growth of the Brazilian peppertree if released in Florida.     

Supplementary host specificity testing of the sawfly <Emphasis Type="Italic">Heteroperryia hubrichi</Emphasis>, a candidate for classical biological control of Brazilian peppertree, <Emphasis Type="Italic">Schinus terebinthifolius</Emphasis>, in the USA

Supplementary host specificity tests were conducted with the defoliating sawfly Heteroperreyia hubrichi (Hymenoptera: Pergidae), a candidate for classical biological control of Brazilian peppertree, Schinus terebinthifolius (Sapindales: Anacardiaceae), in the United States. These tests were conducted as part of the environmental assessment required by the National Environmental Policy Act (NEPA). The suitability of the federally listed endangered native plant Rhus michauxii (Anacardiaceae) and the economically important Litchi chinensis (Sapindaceae) as potential host plants for H. hubrichi was evaluated in a series of no-choice larval development tests conducted in a Florida quarantine laboratory. Neonate larvae transferred to individual test plants failed to develop to the pupal stage on R. michauxii or L. sinensis, whereas Brazilian peppertree supported development of the sawfly to pupation. The results of the additional host specificity tests indicated these critical non-target plants are not at risk from attack by H. hubrichi if it were released in Florida, USA.     

Biology and host range of Omolabus piceus, a weevil rejected for biological control for Schinus terebinthifolius in the USA

Surveys for biological control agents of the invasive weed Schinus terebinthifolius (Anacardiaceae) discovered two Omolabus weevils (Coleoptera: Attelabidae) feeding on the plant in its native range. Molecular and morphological analysis indicated that one of these species consistently fed on the target weed and the other species fed more broadly. Aspects of the biology and host range of the more specific species, Omolabus piceus (Germar) were examined to determine its suitability as a biological control agent of S. terebinthifolius in the USA. Adults feed on newly formed leaves, and eggs, larvae and pupae develop in curled fragments of leaves, called nidi. Larvae consumed an average of 11.3 (±0.4) mg throughout their development which required 15.1 (±0.2) days. An average of 31.6 (±2.7) eggs were laid per female during their 23.8 (±2.2) day lifetime, after a 3.4 (±1.0) day preoviposition period. In no-choice tests, O. piceus adults fed and oviposited on all tested native North American, Caribbean and agricultural Anacardiaceae species except for M. indica. The field host-range of O. piceus, as determined by samples of host use in the native range, included three Schinus, two Lithrea and one Anacardium species. Therefore, we do not recommend O. piceus for biological control of S. terebinthifolius in the USA. However, the utilization of this species in other infested areas such as Hawaií and Australia should be considered.     

Effect of herbivory on growth and biomass allocation of Brazilian peppertree (Sapindales: Anacardiaceae) seedlings in the laboratory

Brazilian peppertree (Schinus terebinthifolius Raddi), native to South America, is invading many ecosystems in south and central Florida. The defoliating tortricid moth Episimus unguiculus Clarke was selected as a potential biocontrol agent of Brazilian peppertree in Florida. The objective of this study was to examine the effect of different levels of herbivore damage on growth and biomass allocation of Brazilian peppertree seedlings in the laboratory. Three treatments were established: (1) no herbivory (control), (2) low herbivory (~4 larvae/plant), and (3) high herbivory (~12 larvae/plant). High levels of herbivory significantly reduced the number of leaflets, plant height, foliar biomass, foliar relative growth rate (RGR) and shoot: root ratio of Brazilian peppertree seedlings. Moreover, plants were not able to recover from herbivory after 2 months. The performance of Brazilian peppertree subjected to low herbivory levels did not differ from the control plants (no herbivory). The potential effectiveness of the biocontrol agent E. unguiculus to suppress this noxious weed is examined.     

Predicting the host range of Nystalea ebalea: Secondary plant chemistry and host selection by a surrogate biological control agent of Schinus terebinthifolia

The safety of weed biological control depends upon the selection and utilization of the target weed by the agent while causing minimal harm to non-target species. Selection of weed species by biological control agents is determined by the presence of behavioral cues, generally host secondary plant compounds that elicit oviposition and feeding responses. Non-target species that possess the same behavioral cues as found in the target weed may be at risk of damage by classical biological control agents. Here we conducted host range tests and examined secondary plant compounds of several test plant species. We studied the specialist herbivore Nystalea ebalea (Lepidoptera: Notodontidae) a Neotropical species, present in Florida as a surrogate biological control agent of the weed, Brazilian peppertree Schinus terebinthifolia, invasive in Florida and Hawaii. We found that the larvae had the greatest survival when fed the target weed, the Neotropical species Spondias purpurea, the Florida native species Rhus copallinum, and the ornamental Pistacia chinensis. Reduced survival and general larval performance were found on the native species Metopium toxiferum and Toxicodendron radicans. Both the volatiles and the allergen urushiols were chemically characterized for all species but urushiol diversity and concentration best predicted host range of this herbivore species. These results provide insight into host selection and utilization by one oligophagous Schinus herbivore. Other potential biological control agents may also be sensitive to plants that contain urushiols and if so, they may pose minimal risk to these native species.     

Diversity and impact of herbivorous insects on Brazilian peppertree in Florida prior to release of exotic biological control agents

Brazilian peppertree, Schinus terebinthifolia Raddi (Anacardiaceae), is a South American plant that is highly invasive in Florida. The impact of insect herbivores on the performance of Brazilian peppertree was evaluated at two locations in Florida using an insecticide exclusion method. Although 38 species of insect herbivores were collected on the invasive tree, there were no differences in growth or reproductive output of insecticide protected and unprotected trees, providing evidence that insect feeding had no measurable impact on tree performance. The majority of insects collected on Brazilian peppertree were generalists, and several were serious agricultural pests.     

The tortoise beetle Physonota maculiventris (Chrysomelidae: Cassidinae) is suitable for release against the weedy Mexican sunflower Tithonia diversifolia (Asteraceae) in South Africa

The biology and host range of the defoliating beetle Physonota maculiventris Boheman (Chrysomelidae: Cassidinae) were studied in quarantine to determine its suitability for release as a biological control agent against Mexican sunflower, Tithonia diversifolia (Hemsl.) A. Gray (Asteraceae), in South Africa. Females laid 5.25?±?0.25 (mean?±?SE) egg batches during their lifetimes, with each batch consisting of approximately 33 eggs. Larvae were highly gregarious as early instars and both larvae and adults fed voraciously, often defoliating the plants completely. The life cycle of the beetle was completed in 67.5?±?7.5 days under quarantine conditions. Among the 58 test plant species subjected to no-choice tests, P. maculiventris developed successfully on T. diversifolia and some sunflower (Helianthus annuus L.) cultivars. However, only minor damage was recorded on non-target species, notably the exotic weed Xanthium strumarium L. and some H. annuus cultivars. Also, survival to adulthood was considerably lower on sunflower cultivars than on the target weed during these tests. During choice tests, P. maculiventris oviposited and developed successfully on T. diversifolia only, with only minor feeding damage on some H. annuus cultivars, suggesting that the beetle’s field host range will be confined to the target weed. Risk analysis also showed that P. maculiventris presents an extremely low risk to non-target plant species (e.g. within the tribe Heliantheae and other close relatives). The study concluded that P. maculiventris is safe for release in South Africa and an application for its release is being considered by the relevant South African regulatory authorities.     

Lifecycle of Rhipicephalus haemaphysaloides under laboratory conditions

Rhipicephalus haemaphysaloides Supino, 1897 (Ixodida: Ixodidae) is a three‐host hard tick widely distributed in Sri Lanka. The lifecycle of the R. haemaphysaloides population in Sri Lanka was studied under laboratory conditions using fully engorged females collected from dogs. Larvae, nymphs and adults were reared on New Zealand rabbits. Engorged females weighed a mean ± standard deviation (SD) of 470.1 ± 106.5 mg and laid a mean ± SD of 4067.4 ± 3136.2 eggs within 16.1 ± 3.7 days. The mean ± SD preoviposition period was 6.5 ± 1.1 days. The mean ± SD reproductive efficiency index was 8.5 ± 4.1, and was higher in heavier females (Pearson correlation, r = 0.8; P = 0.001). The incubation period of eggs was shorter at higher temperatures. The majority (86.9%) of larvae successfully moulted after a mean ± SD premoulting period of 7.9 ± 0.7 days following a parasitic period of 3.2 ± 0.5 days. Unfed larvae survived a mean ± SD of 103.4 ± 19.8 days. Nymphs completed the bloodmeal after 3.7 ± 0.9 days, weighed 5.7 ± 1.7 mg and demonstrated a premoulting period of 15.1 ± 1.9 days. Unfed nymphs survived a mean ± SD of 45.8 ± 3.8 days. Heavier nymphs moulted into females, whereas lighter nymphs moulted into males (two‐sample t‐test, P < 0.001). The bodyweight of adult females increased more than 100‐fold after feeding. The lifecycle of R. haemaphysaloides was successfully completed on rabbits within a mean of 91.3 days (range: 69–117 days) under laboratory conditions.     

Biology and host range of Ophiomyia camarae Spencer (Diptera: Agromyzidae), a potential biocontrol agent for Lantana spp. (Verbenaceae) in Australia

The life history and host range of the herringbone leaf-mining fly Ophiomyia camarae, a potential biological control agent for Lantana spp., were investigated. Eggs were deposited singly on the underside of leaves. Although several eggs can be laid on a single leaf and a maximum of three individual mines were seen on a single leaf, only one pupa per leaf ever developed. The generation time (egg to adult) was about 38 days. Females (mean 14 days) lived longer than males (mean 9 days) and produced about 61 mines. Oviposition and larval development occurred on all five lantana phenotypes tested. Eleven plant species representing six families were tested to determine the host range. Oviposition and larval development occurred on only lantana and another nonnative plant Lippia alba (Verbenaceae), with both species supporting populations over several generations. A CLIMEX model showed that most of the coastal areas of eastern Australia south to 30°16′ S (Coffs Harbour) would be suitable for O. camarae. O. camarae was approved for release in Australia in October 2007 and mines have been observed on plants at numerous field sites along the coast following releases.     

The Brazilian peppertree seed-borne pathogen,Neofusicoccum batangarum,a potential biocontrol agent

The invasive exotic Brazilian peppertree, Schinus terebinthifolius Raddi (Sapindales: Anacardiaceae) has become a serious threat to the delicate ecosystem of Everglades National Park in Florida, USA. More than 4000 ha in the Hole-in-the-Donut (HID) area within the park have been infested with Brazilian peppertree. Brazilian peppertree is a prolific seed producer, which enhances its invasive potential. Native phytopathogens can be a viable tool in the management of exotic species; no prior studies have reported on the occurrence of native seed-borne pathogens of Brazilian peppertree in Florida. This study showed that drupes of Brazilian peppertree are affected by seed-borne fungal pathogens. These fungal pathogens either cause germination failure or attack seedlings after germination, which results in reduced vigor or seedling death. The seed-borne fungal isolate BPSPF-1 was found to be virulent, and when inoculated it was able to kill Brazilian peppertree seedlings in seedling assays, and 1 year old saplings in greenhouse trials. Field inoculation of Brazilian peppertree branches with BPSPF-1 resulted in dieback symptoms. Host range studies on one related native species (winged sumac, Rhus copallinum) and one non-native species (mango, Mangifera indica) showed that neither was affected by girdle inoculation of stems. The BPSPF-1 isolate produced dark melanized mycelium on agar media and did not produce conidia or other fruiting structures. Based on ITS DNA sequence analyses, the isolate was identified as Neofusicoccum batangarum.     

Multiple host use by a sap-sucking membracid: population consequences of nymphal development on primary and secondary host plant species

Aconophora compressa is a gregarious, sap-sucking insect that uses multiple host plant species. Nymphal host plant species (and variety) significantly affected nymphal survival, nymphal development rate and the subsequent size and fecundity of adults, with fiddlewood (Citharexylum spinosum) being significantly best in all respects. Nymphs that developed on a relatively poor host (Duranta erecta var “geisha girl”) and which were moved to fiddlewood as adults laid significantly fewer eggs (mean ± SE = 836 ± 130) than those that developed solely on fiddlewood (1,329 ± 105). Adults on geisha girl, regardless of having been reared as nymphs on fiddlewood or geisha girl, laid significantly fewer eggs (342 ± 83 and 317 ± 74, respectively) than adults on fiddlewood. A simple model that incorporates host plant related survival, development rate and fecundity suggests that the population dynamics of A. compressa are governed mainly by fiddlewood, the primary host. The results have general implications for understanding the population dynamics of herbivores that use multiple host plant species, and also for the way in which weed biological control host testing methods should be conducted. Handling Editor: Robert Glinwood     

A promising biological control agent for the invasive alien plant,Pereskia aculeata Miller (Cactaceae), in South Africa

Pereskia aculeata Miller (Cactaceae) is an invasive alien plant from Central and South America that has become a problematic environmental weed in South Africa. A potential biological control agent, the stem-wilter, Catorhintha schaffneri Brailovsky & Garcia (Coreidae), was collected in southern Brazil and imported into quarantine in South Africa. Field host range data suggested that C. schaffneri has a host range restricted to P. aculeata. No-choice nymph survival tests were then conducted on 27 test plant species in 9 families. Survival to the adult stage was only recorded on P. aculeata and the closely related Pereskia grandifolia Haw. (Cactaceae). Mortality was significantly higher on P. grandifolia with only 3% of the nymphs reaching the adult stage compared with 74% on P. aculeata indicating that P. aculeata is the primary host plant. P. grandifolia is native in South America and is of no agricultural importance in South Africa so any feeding on P. grandifolia in South Africa would have no negative environmental or economic consequences. In other tests, adult survival on P. aculeata [25.8 days (SE ± 3.74)] was significantly longer than on other test plant species [4.3 days (SE ± 0.36)] further confirming the host specificity of the species. Impact studies conducted in quarantine indicated that C. schaffneri is damaging to P. aculeata, significantly reducing the number of leaves and the shoot lengths of plants, even at relatively low insect densities. C. schaffneri is safe for release in South Africa and is likely to be a damaging and effective agent.     

Control of Pseudophilothrips ichini (Thysanoptera: Phlaeothripidae) with acephate to exclude a biological control agent of Schinus terebinthifolia

Post-release monitoring of biological control agents to determine impact on the target weed has recently received increased priority. Several methods are available to measure the impact of a biological control agent by manipulating the agent population while measuring fitness of the weed. Brazilian peppertree, Schinus terebinthifolia is one of the most damaging weeds in subtropical areas of Florida and Hawaii. A biological control agent, the thrips, Pseudophilothrips ichini is a sap-feeder that shows high levels of specificity and causes severe distortion of leaf tips of the weed. Thrips populations of this species and a generalist thrips, the red banded thrips Selenothrips rubrocinctus were experimentally manipulated by applications of the systemic insecticide acephate by both foliar applications and by an inserted encapsulated formulation. Foliar applications protected plants against red banded thrips for 29 days and against the biological control thrips, P. ichini for 22 days after treatment. Control with inserts were initially low but was achieved after 60 days and this control continued for 182 days after treatment. Manipulation of these biological control thrips populations with foliar or inserted formulations will assist in the determination of biological control agent impact.     

Laboratory biology and impact of a stem-boring weevil Apocnemidophorus pipitzi (Coleoptera: Curculionidae) on Schinus terebinthifolia

Brazilian peppertree, Schinus terebinthifolia Raddi (Anacardiaceae), was introduced into Florida, USA, from South America as an ornamental plant in the late 19th and early 20th centuries. It eventually escaped cultivation and is a serious threat to the state’s biodiversity. In the 1980s, this invasive weed was targeted for classical biocontrol. Surveys for natural enemies of Brazilian peppertree conducted in the native range resulted in the discovery of several candidate biocontrol agents. A stem-boring weevil identified as Apocnemidophorus pipitzi (Faust) was collected in Paraguay and transported under permit to Florida, USA. A laboratory colony of A. pipitzi was established in April 2007 by caging adults on cut branches of Brazilian peppertree supplemented with leaf bouquets. Adults are defoliators that feed mainly on the upper surface of subterminal leaflets. Females deposit eggs singly inside the stems and larvae feed under the bark where they damage the vascular cambium. There are five instars, pupation occurs inside the stem and a new generation is produced in 3–4 months. Growth of potted plants with and without exposure to weevil herbivory was compared over an 11-month period. Feeding damage by adults and larvae significantly increased leaf abscission and reduced leaf and root biomass accumulation.