The leafmining Leurocephala schinusae (Lepidoptera: Gracillariidae): not suitable for the biological control of Schinus terebinthifolius (Sapindales: Anacardiaceae) in continental USA

The host range of Leurocephala schinusae Davis & Mc Kay (Lepidoptera: Gracillariidae) was studied to assess its suitability as a biological control agent of Schinus terebinthifolius Raddi (Anacardiaceae), a serious environmental weed in the USA and elsewhere in the world. The host range was determined in the laboratory with adult no-choice oviposition (Argentina and USA) and larval development tests (USA). Seventeen plant species in ten genera were selected based on taxonomic relatedness to S. terebinthifolius, economic importance, and availability. Additional information was obtained by sampling foliage of S. terebinthifolius and six other South American native Anacardiaceae species in north-eastern Argentina. In the laboratory, except for Lithrea molleoides and Spondias mombin, all of the tested species were accepted for oviposition with a marked preference for Rhus aromatica. Incipient mines successfully developed into complete mines, pupae and adults on R. aromatica, Rhus copallinum, Schinus molle, Schinus lentiscifolius and S. terebinthifolius. In the field, although L. schinusae showed a clear preference for S. terebinthifolius, the host range, as determined by samples of host use in the native range, included three other Schinus species (S. lentiscifolius, Schinus longifolius, Schinus weinmannifolius) and one Astronium species (Astronium balansae). In conclusion, L. schinusae will not be considered for the biological control of S. terebinthifolius in continental US. However, the utilisation of this species in other infested areas such as Hawaii and Australia should be further discussed.     

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.     

Biology, host specificity tests, and risk assessment of the sawfly Heteroperreyia hubrichi, a potential biological control agent of Schinus terebinthifolius in Hawaii

Heteroperreyia hubrichiMalaise (Hymenoptera: Pergidae), a foliagefeeding sawfly of Schinusterebinthifolius Raddi (Sapindales:Anacardiaceae), was studied to assess itssuitability as a classical biological controlagent of this invasive weed in Hawaii. No-choice host-specificity tests were conductedin Hawaiian quarantine on 20 plant species in10 families. Besides the target weed, adultfemales oviposited on four test species. Females accepted the Hawaiian native Rhussandwicensis A. Gray (Sapindales:Anacardiaceae) as an oviposition host equallyas well as the target species. The other threespecies received significantly fewer eggs. Neonate larvae transferred onto test plantssuccessfully developed to pupae on S.terebinthifolius (70% survival) and R.sandwicensis (1% survival). All other 18test plant species failed to support larvaldevelopment. A risk analysis was conducted toquantify the acceptability of non-targetspecies as host plants for H. hubrichi onthe basis of the insect's performance atvarious stages in its life cycle. Risk ofdamage to all plant species tested wasinsignificant except for R. sandwicensis. Risk to this native plant relative to S.terebinthifolius was estimated at 1%. Currently this level of risk is too high torequest introduction of this insect into theHawaiian environment. Detailed impact studiesin the native range of S. terebinthifoliusare needed to identify thepotential benefit that this insect offers. Also, field studies in South America withpotted R. sandwicensis would give a morereliable analysis of the risk this nativeHawaiian plant would face from naturalpopulations of H. hubrichi.     

Host range tests reveal Paectes longiformis is not a suitable biological control agent for the invasive plant Schinus terebinthifolia

The most critical step during a weed biological control program is determination of a candidate agent’s host range. Despite rigorous protocols and extensive testing, there are still concerns over potential non-target effects following field releases. With the objective to improve risk assessment in biological control, no-choice and choice testing followed by a multiple generation study were conducted on the leaf-defoliator, Paectes longiformis Pogue (Lepidoptera: Euteliidae). This moth is being investigated as a biological control agent of Schinus terebinthifolia Raddi (Sapindales: Anacardiaceae), which is one of the worst invasive plant species in Florida, USA. Results from no-choice testing showed higher larval survival on S. terebinthifolia (48 %) and its close relative Schinus molle L. (47 %), whereas lower survival was obtained on six non-target species (<25 %). When given a choice, P. longiformis females preferred to lay eggs on the target weed, but oviposition also occurred on four non-target species. An improved performance on the native Rhus aromatica Aiton was found when insects were reared exclusively on this non-target species for one or two generations. Results from host range testing suggest that this moth is oligophagous, but has a preference for the target weed. Non-target effects found during multiple generation studies indicate that P. longiformis should not be considered as a biological control agent of S. terebinthifolia.     

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.     

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.     

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.     

Biology and host range of Heterapoderopsis bicallosicollis: a potential biological control agent for Chinese tallow Triadica sebifera

Chinese tallow, Triadica sebifera, is an invasive weed that infests natural and agricultural areas of the south-eastern USA. A candidate insect for biological control of Chinese tallow has been studied under quarantine conditions. The biology and host range of a primitive leaf-feeding beetle, Heterapoderopsis bicallosicollis, were examined between July 2008 and February 2010. H. bicallosicollis adults fed on 16 of 29 non-target species and survived >10 days on all 29 species, more than the number of days that adults survived when deprived of food. Additionally, adult feeding, oviposition and partial larval development occurred on a Florida endangered species, Heterosavia bahamensis. These data indicated that H. bicallosicollis adult feeding and oviposition may not be limited to the target weed and included several valued North American natives. Therefore, as its release could pose unacceptable risks, testing of this species was discontinued and the quarantine colony destroyed.     

Host specificity testing and examination for plant pathogens reveals that the gall‐inducing psyllid Calophya latiforceps is safe to release for biological control of Brazilian peppertree

Brazilian peppertree, Schinus terebinthifolia Raddi (Anacardiaceae), is one of the worst upland exotic weeds in Florida, USA. Foreign exploration for natural enemies led to the discovery of a pit‐galling psyllid, Calophya latiforceps Burckhardt (Hemiptera: Calophyidae), in the state of Bahia, Brazil, in 2010. Crawlers of C. latiforceps stimulate the formation of galls on the leaves of S. terebinthifolia resulting in leaf discoloration and in some cases leaf abscission. To determine whether C. latiforceps is a safe candidate for biological control of S. terebinthifolia, host specificity and the presence of selected plant pathogens were examined. Adult oviposition, gall formation, and adult survival of C. latiforceps were examined on 89 plant species under no‐choice and choice conditions. We found that C. latiforceps laid eggs on plants in seven families; however, crawlers stimulated gall formation and completed development to adult only on S. terebinthifolia. All crawlers on non‐target plants died, likely due to starvation caused either by the absence of a feeding stimulus or by a hypersensitive plant response. Under no‐choice conditions, 10% of adults lived for 19 days on the target weed, but adult survival was reduced to <3 days on non‐target plants. Choice testing revealed that females preferred to oviposit on S. terebinthifolia compared to non‐target plants. Molecular methods and indicator host inoculations did not detect the presence of ‘Candidatus Liberibacter solanacearum’, ‘Ca. L. asiaticus’, ‘Ca. L. americanus’, ‘Ca. L. africanus’, or plant viruses in adult C. latiforceps. We conclude that releasing C. latiforceps in the USA will have extremely low risk to non‐target plants, and provides another tool for the management of S. terebinthifolia.     

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.     

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.     

Risk assessment of Episimus unguiculus (Lepidoptera: Tortricidae), a biological control agent of Schinus terebinthifolia (Sapindales: Anacardiaceae) in Hawaii,USA

Schinus terebinthifolia Raddi (Anacardiaceae) is an introduced ornamental tree from South America that has become one of the most invasive weeds in Hawaii and Florida, USA. Exploratory surveys in the plant’s native range from 1950 to 2014 identified several potential biological control agents. One of these is the leaflet rolling moth Episimus unguiculus Clarke (Lepidoptera: Tortricidae), previously known as Episimus utilis Zimmerman. This biological control agent was released in Hawaii in the 1950s where high densities were occasionally observed, leading to partial control of S. terebinthifolia by the 1960s. Larvae are leaf tiers capable of completely defoliating small plants. In order to investigate the release of E. unguiculus in the continental USA, a series of laboratory no- choice, and multiple-choice tests were conducted in Florida, and a preliminary open field test with a native plant in Hawaii. Under the confined laboratory conditions imposed during the no-choice tests, E. unguiculus accepted the economically important Pistacia spp. and several other non-target plants for oviposition and development. However, in the multiple-choice tests E. unguiculus exhibited a clear preference for S. terebinthifolia relative to non-target plants accepted in the no-choice tests. Overall, the results of field observations during surveys in South America and Hawaii and host range studies completed in Hawaii and Florida showed that E. unguiculus is a narrow specialist on S. terebinthifolia, its natural host plant.     

Host specificity of Metriona elatior, a potential biological control agent of tropical soda apple, Solanum viarum, in the USA

The leaf beetle Metriona elatior from Brazil-Argentina was screened in the Florida (USA)State quarantine facility as a potential biological control agent of tropical soda apple, Solanum viarum, a recently arrived weed species. Multiple-choice host-specificity tests were conducted in small cages (60 cm × 60 cm × 60 cm) using 95 plant species in 29 families. Adults fed heavily on the main target weed (S. viarum), and on turkey berry,Solanum torvum (noxious weed of Asiatic origin); fed moderately on red soda apple, Solanum capsicoides (weed of South American origin), and eggplant, Solanum melongena (economic crop); and fed lightly on aquatic soda apple, Solanum tampicense (weed of Mexican-Caribbean-Central American origin), and onsilverleaf nightshade, Solanum elaeagnifolium(native weed widely distributed). M.elatior adults laid 84 to 97% of their egg masses onS. viarum, and 3 to 16% on S. melongena. Non-choice host-specificity tests were also conducted in quarantine in which M. elatior adults and neonate larvae were exposed to 17 and 19 plant species, respectively. Tests with the neonates indicate that this insect was able to complete its development on S. viarum, S. torvum, S. melongena, and S. capsicoides. Although some adult feeding and oviposition occurred on S.melongena in quarantine on potted plants in small cages, no feeding or oviposition by M. elatiorwas observed in field experiments conducted in Brazil. Surveys in unsprayed S. melongena fields in Argentina and Brazil indicated that M. elatioris not a pest of S. melongena in South America. The evidence obtained from the South-American field surveys, Brazil open-field experiments, and Florida quarantine host specificity tests indicate that M. elatior causes significant feeding damage toS. viarum, and does not represent a threat to S. melongena crops in the USA. Therefore an application for permission to releaseM. elatior against S. viarum in the USA was submitted in October 1998. This revised version was published online in July 2006 with corrections to the Cover Date.     

Larval host plants of two lizard beetles in the genus Tetraphala (Coleoptera,Erotylidae, Languriinae,Languriini) from Taiwan,with a host plant list of Languriini

Lizard beetles (Erotylidae, Languriinae, Languriini) are known as stem borers of plants and contain agricultural pests and endangered species, but their species–host plant associations have been poorly documented. Here we investigated the larval host plants of two species of the genus Tetraphala Strum, T. collaris (Crotch) and Tetraphala sp. occurring in Taiwan. Females of T. collaris excavated living leafstalks and stems of the herbaceous dicot, Sambucus chinensis (Adoxaceae) using their mandibles for oviposition. We observed the eggs and early-instar larvae inside and nearby oviposition holes and late-instar larvae inside stems, suggesting that T. collaris uses living leafstalks and stems of S. chinensis as oviposition substrate and the larvae tunnel into stems with feeding on the tissues. Similarly, females of Tetraphala sp. excavated living leafstalks of the fern, Pteris wallichiana (Pteridaceae) using their mandibles for oviposition. We observed the eggs and early-instar larvae inside and nearby oviposition holes. When reared in laboratory, a larva reached adulthood inside the leafstalk. These results indicated that Tetraphala sp. uses living leafstalks of Pt. wallichiana as oviposition substrate and the larvae complete their development within. This study revealed that the genus Tetraphala contains both fern- and dicot-users during larval period. Further study is needed to clarify the evolutionary process of host plant use of languriines. Additionally, the host plant list of Languriini is provided.     

Defoliating broad-nosed weevil,Plectrophoroides lutra; not suitable for biological control of Brazilian pepper (Schinus terebinthifolius)

Adults of the weevil Plectrophoroides lutra were evaluated for biological control of Schinus terebinthifolius. No-choice tests conducted on North American and other valued plants indicated the adults fed on all species offered. Thus, it is unlikely that P. lutra will be developed as a biological control for S. terebinthifolius.     

Recruitment of the invasive ornamental,Schinus terebinthifolius,is dependent upon frugivores

Abstract Generalist avian frugivores often play an important role in the processes of naturalization and invasion for plants introduced for ornamental and landscaping purposes. We investigated the potential role of Australian birds in the current invasion of riparian habitats and coastal wetlands by the ornamental Schinus terebinthifolius Raddi. Feeding trials in captivity predicted silvereyes (Zosterops lateralis Latham) as dispersal vectors for this weed. There were no differences in either total germination or germination rate between seeds voided by caged silvereyes and those from which exocarps had been removed manually. Germination of seeds incubated within entire fruits was minimal, as was emergence from intact fruits in a field experiment. Seed banks of S. terebinthifolius were relatively transient under field conditions, with no seeds surviving for 9 months. Since fewer than 5% of the seeds in sown whole fruits gave rise to seedlings (cf. 20–42% for sown bare seeds), we conclude that recruitment potential of S. terebinthifolius is highly dependent upon the consumption of its fruits by frugivores.     

Life history and host range of Sauris nr. purpurotincta,an unsuitable biological control agent for Chinese tallowtree

Foreign surveys in China discovered a defoliating insect species feeding on the leaves of Chinese tallowtree (Triadica sebifera), an invasive weed of the southeastern U.S.A. The life history of this species, Sauris nr. purpurotincta (Lepidoptera: Geometridae), was examined and larval no-choice and adult multiple-choice host range tests were conducted in quarantine to evaluate their suitability for biological control of Chinese tallowtree. The results indicated that the larvae have five instars and require approximately 22 days to complete development to the adult stage. Host range tests indicated that the larvae could not feed and complete development on most species tested. However, 40% of the larvae survived when fed leaves of Hippomane mancinella, a state-listed endangered species in Florida, and all larvae survived when fed Morella cerifera, a common native species of the southeastern U.S.A. Multiple-choice oviposition tests indicated eggs were laid on leaves of both a south Florida native plant Gymnanthes lucida and Chinese tallowtree. Considering this broad host range, this species will not be considered further for biological control of Chinese tallowtree in the U.S.A.     

Relationships of herbivore feeding and plant flavonoids (Coleoptera: Chrysomelidae and Anacardiaceae: Rhus)

Summary Eighteen leaf flavonoid compounds were isolated from several populations of Rhus tripartita from xeric habitats in Israel, ornamental Schinus terebinthifolius from Israel, and three species of Rhus (vulgaris, natalensis, tenuinervis) from mesic habitats in Kenya. Foodplant preference testing of Rhus-feeding Leaf Beetles (Blepharida sacra from Israel and B. marginalis and B. conradsi from Kenya) correlated well with the flavonoid composition of the different foodplants. Blepharida sacra and B. marginalis foodplant preferences demonstrated an herbivore sibling relationship but there is evidence, including foodplant ecology and distribution, that they are separate species. The herbivorefoodplant coevolution of the xeric B. sacra-R. tripartita is distinct from that of the mesic B. marginalis-R. vulgaris/natalensis, however, this study also indicates possible ancestral relationships between the herbivore species as well as between the plant species.     

Essential oils of Schinus terebinthifolius and S. molle (Anacardiaceae): Mitodepressive and aneugenic inducers in onion and lettuce root meristems

Essential oils constitute an important group of plant products and include a mixture of volatile low-molecular-weight terpenes. The present study aimed to determine the phyto- and cytotoxicity of essential oils from leaves of Schinus molle and Schinus terebinthifolius on lettuce and onion. These essential oils affected germination, initial growth, and mitotic and metaphasic indexes of the target species. Compared to negative controls, essential oils of S. molle and S. terebinthifolius reduced the mitotic index of onion by 21.05% and 82.03%, respectively. Similar results were observed for lettuce. The volatiles also induced chromosomal abnormalities such as spindle disturbance at late prophase, sticky metaphase, c-mitosis, micronucleus, and nuclear buds. Although the essential oils of both species shared the same major compound (α-pinene), more pronounced effects were observed in S. terebinthifolius treatments. The results suggest that major and minor compounds of these essential oils act in synergy, causing the inhibitory effects observed on onion and lettuce.