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.     

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.     

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.     

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.     

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.     

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.     

Life history and host range of Oxydia vesulia transpeneus,an unsuitable biological control agent of Brazilian peppertree

The suitability of Oxydia vesulia transpeneus (Cramer) (Lepidoptera: Geometridae) was assessed as a potential biological control agent of the invasive weed Brazilian Peppertree Schinus terebinthifolia Raddi. Larvae were collected in Brazil feeding on the plant in its native range and colonised in quarantine where life history and host range studies were conducted (27?±?2°C; 50RH). Development time from neonate to adults when fed Brazilian peppertree leaves was 48.0 (±2.2) days for females and 51.0 (±1.3) days for males. Larvae generally required five (occasionally six) instars to reach the adult stage. Females had greater pupal weights 1004.1 (±45.9) mg compared with males 668.5 (±19.7) mg. Larvae were tested on seven non-target plant species from Florida natives, ornamentals, to economic species. Larvae completed development on all but one of these valued plant species. These results suggest that the host range of O. vesulia is not sufficiently specific for release as a biological control against Brazilian peppertree in the USA.     

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.     

Molecular and morphological examination of Cyrtobagous sp. collected from Argentina, Paraguay, Brazil, Australia, and Florida

Two members of the floating fern genus Salvinia (Salviniaceae), S. minima Baker and S. molesta Mitchell, have established in the United States. Cyrtobagous salviniae Calder and Sands (Coleoptera: Curculionidae), long established on Florida S. minima, was released in Texas and Louisiana as a biocontrol agent for both species. Subsequently, sequence analysis of the 28S rRNA D2 expansion domain suggested that the Florida and Brazilian populations (used worldwide for biocontrol) of C. salviniae might constitute two cryptic species. In response, the Brazilian weevil was imported from Australia and released instead onto S. molesta. We sampled C. singularis Hustache and C. salviniae from their native ranges in Brazil, Argentina, and Paraguay and sequenced them (D2) along with Australian and Florida samples. The genetic distance between C. singularis and C. salviniae samples is much greater (almost 5×) than the distance between either the Florida and Brazilian samples or the Brazilian and Argentinean/ Paraguayan C. salviniae samples. Since C. singularis and C. salviniae are cryptic species, the Florida and Brazilian populations (or for that matter Brazilian and Argentinean/Paraguayan) could reasonably be described as demes or ecotypes. Occurrence data indicates that, in parts of their ranges, C. salviniae and C. singularis are not only sympatric but also feed on the same plant species at the same site. While host adaptation (species preferences) likely occurs within local demes, both species seem capable of adapting to the available resource (Salvinia species). Finally, a polymerase chain reaction (PCR) primer was developed to distinguish the Florida and Brazilian/Australian types.     

Influence of host-plant quality on the performance of <Emphasis Type="Italic">Episimus unguiculus</Emphasis>, a candidate biological control agent of Brazilian peppertree in Florida

Brazilian peppertree, Schinus terebinthifolius Raddi (Sapindales: Anacardiaceae), introduced from South America, invades a variety of habitats in Florida (e.g. disturbed sites, coastal mangrove forests). The objective of this study was to evaluate the effect of host-plant quality on the performance of Episimus unguiculus Clarke (=E. utilis Zimmerman) (Lepidoptera: Tortricidae), a potential biocontrol agent of Brazilian peppertree. Experiments were conducted in the laboratory using Brazilian peppertrees exposed either to different salinity levels (0, 6, 12 parts per thousand), or to different nutrient levels (low, medium, high). Higher survival (55%) and faster development (32 day) to adulthood was observed on plants grown in fresh-water environments (0 ppt) compared to low (6 ppt) or high-salinity environments (12 ppt). In addition, higher survival (40%), faster development (34 day) and higher fertility (88% eggs hatched) occurred in high-nutrient treatments. Based on these results, field releases should be conducted in favorable habitats (e.g., low salinity, high fertility soils) to maximize the possibility of establishment and population growth of E. unguiculus in Florida. Handling Editor: John Scott.     

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.     

Impact in quarantine of the galling weevil Lepidapion argentatum on shoot growth of French broom (Genista monspessulana), an invasive weed in the western U.S.

In weed biocontrol, there is a need for pre-release efficacy assessments for potential agents. Genista monspessulana ((L.) L. A. S. Johnson (Fabaceae), French broom) is an invasive perennial shrub in the western U.S. The galling weevil Lepidapion argentatum Gerstaecker is a potential biocontrol agent. The impact of increasing weevil density on galling damage, plant height, width, leaf damage, and relative growth rate (RGR) was assessed in greenhouse experiments on two to three-month-old seedlings infested with either one or three weevils. Infestation by three female weevils caused 48% more galls producing 27% more larvae than did infestation with one female while causing only 1% leaf damage and no difference in total leaf area. Infestation with multiple weevils caused a 55% and 29% decrease in plant height and canopy width respectively, while single-weevil infestation decreased height by 32% and width to the same degree as for multiple weevils. The RGR of seedlings infested with three weevils was three times slower than the controls, while growth was reduced 2-fold by single-weevil infestation. Reductions in plant size and growth rate induced by weevil galling could reduce plant competitive survival to reproduction and also plant population dispersal as seedlings. Our results suggest that L. argentatum has the potential to cause impact to French broom seedlings if released in the invasive range.     

Colonization patterns of the invasive Brazilian peppertree, Schinus terebinthifolius, in Florida

Invasive species are believed to spread through a process of stratified dispersal consisting of short-distance diffusive spread around established foci and human mediated long-distance jumps. Brazilian peppertree (Schinus terebinthifolius), native to South America, was introduced twice as an ornamental plant into Florida, USA, just over 100 years ago. A previous study indicated that these two introductions were from genetically differentiated source populations in the native range. In this study, we took advantage of these contrasting genetic signatures to study the spatial spread of Brazilian peppertree across its entire range in Florida. A combination of spatial genetic and geostatistical analyses using chloroplast and nuclear microsatellite markers revealed evidence for both diffusive dispersal and long-distance jumps. Chloroplast DNA haplotype distributions and extensive bands of intra-specific hybridization revealed extensive dispersal by both introduced populations across the state. The strong genetic signature around the original introduction points, the presence of a general southeast to northwest genetic cline, and evidence for short-distance genetic spatial autocorrelation provided evidence of diffusive dispersal from an advancing front, probably by birds and small mammals. In the northernmost part of the range, there were patches having a high degree of ancestry from each introduction, suggesting long-distance jump dispersal, probably by the movement of humans. The evidence for extensive movement throughout the state suggests that Brazilian peppertree will be capable of rapidly recolonizing areas from which it has been eradicated. Concerted eradication efforts over large areas or the successful establishment of effective biocontrol agents over a wide area will be needed to suppress this species.     

Larval <Emphasis Type="Italic">Cryptothelea gloverii</Emphasis> (Lepidoptera: Psycidae), an arthropod predator and herbivore on Florida citrus

The orange bagworm (OBW), Cryptothelea gloverii (Packard) (Lepidoptera: Psychidae) was previously reported feeding on citrus fruit and foliage and preying upon the camphor scale Pseudaonidia duplex (Cockerell) (Homoptera: Coccidae). In this study using laboratory assays, OBW preyed upon citrus rust mite, Phyllocoptruta oleivora (Ashmead) (Acari: Eriophyidae) and consumed eggs and adults of both P. oleivora and Panonychus citri (McGregor) (Acari: Tetranychidae), two important pest mites on Florida citrus. OBW was also observed to feed on the purple scale, Lepidosaphes beckii (Newman) (Homoptera: Diaspididae) and on a fungus (Penicillium sp.). OBW fed on orange and grapefruit leaves by starting from the border and eating part of the leaf, by chewing holes, or consuming the outer epithelium of either the axial or abaxial surface of the leaf without penetrating through the leaf. OBW was observed in orange orchards in association with fruit extensively russeted by P. oleivora feeding. Laboratory assays revealed that OBW larvae preferred to feed on oranges infested with P. oleivora rather than on clean fruits that were free of mite feeding damage. Feeding damage to citrus fruit by OBW larvae results in one to several holes being eaten into the rind or albedo, without damage to the fruit sacs.     

Larval Cryptothelea gloverii (Lepidoptera: Psycidae), an arthropod predator and herbivore on Florida citrus

The orange bagworm (OBW), Cryptothelea gloverii (Packard) (Lepidoptera: Psychidae) was previously reported feeding on citrus fruit and foliage and preying upon the camphor scale Pseudaonidia duplex (Cockerell) (Homoptera: Coccidae). In this study using laboratory assays, OBW preyed upon citrus rust mite, Phyllocoptruta oleivora (Ashmead) (Acari: Eriophyidae) and consumed eggs and adults of both P. oleivora and Panonychus citri (McGregor) (Acari: Tetranychidae), two important pest mites on Florida citrus. OBW was also observed to feed on the purple scale, Lepidosaphes beckii (Newman) (Homoptera: Diaspididae) and on a fungus (Penicillium sp.). OBW fed on orange and grapefruit leaves by starting from the border and eating part of the leaf, by chewing holes, or consuming the outer epithelium of either the axial or abaxial surface of the leaf without penetrating through the leaf. OBW was observed in orange orchards in association with fruit extensively russeted by P. oleivora feeding. Laboratory assays revealed that OBW larvae preferred to feed on oranges infested with P. oleivora rather than on clean fruits that were free of mite feeding damage. Feeding damage to citrus fruit by OBW larvae results in one to several holes being eaten into the rind or albedo, without damage to the fruit sacs.     

INSECT-CYCAD SYMBIOSIS AND ITS RELATION TO THE POLLINATION OF ZAMIA FURFURACEA (ZAMIACEAE) BY RHOPALOTRIA MOLLIS (CURCULIONIDAE)

Zamia furfuracea, a cycad of Mexican origin, in cultivation is pollinated by the snout weevil, Rhopalotria mollis, also of Mexican origin. This weevil apparently is host specific, swarming upon male cones of the cycad, where mating, feeding, and oviposition occur. Sporophylls of male cones are rich in starch; those of female cones are poor in starch, and weevils feed upon male cones and are visitors to but not feeders upon or within female cones. Pollen transport to female cones occurs during such visitation. All stages of metamorphosis of R. mollis occur within male cones; larvae feed exclusively on parenchyma of microsporophylls, pupate within stalks of microsporophylls, and emerge as adults from the outer ends of microsporophylls. They do not feed on pollen and do not damage microsporangia or pollen. Toward the end of the breeding season of the weevil (and the cycad), some larvae enter diapause in thick-walled pupal cases within microsporangial stalks of pollen-spent cones. These remain in diapause until the next reproductive season of the cycad.     

Laboratory host range testing of Lilioceris sp. near impressa (Coleoptera: Chrysomelidae) – a potential biological control agent of air potato,Dioscorea bulbifera (Dioscoreaceae)

Air potato, Dioscorea bulbifera, is an invasive, herbaceous, climbing vine, which dominates invaded native vegetation in Florida. The fortuitous discovery of Lilioceris sp. near impressa defoliating D. bulbifera vines and feeding on the bulbils (aerial tubers) in the Katmandu Valley of Nepal initiated a project to assess the potential of this leaf beetle for biological control of air potato in Florida. Quarantine host specificity tests were conducted on 41 plant species in 24 families and 13 orders, with 26 species outside of the Dioscoreaceae and 15 species within the Dioscoreaceae. Adults test fed (nibbled) on 4/12 of tested Dioscorea species, but no larval feeding or development occurred on any plant other than the target, D. bulbifera. The larvae feed gregariously and quickly skeletonize offered leaves of air potato. Air potato bulbils that received any feeding damage to the primary meristematic region did not sprout. The ability of the beetle larvae and adults to feed on the bulbils is important because in Florida, the plant rarely flowers or produces fruit, so these aerial tubers are the primary means of persistence and spread. The adults can live for several months without food. This extremely specialized herbivore from part of the weed's native range appears to have great promise as a biological control of air potato.     

The effects of feeding by the rice water weevil, Lissorhoptrus oryzophilus Kuschel, on the growth and yield components of rice, Oryza sativa

Abstract 1 The effects of feeding by larvae of the rice water weevil, Lissorhoptrus oryzophilus Kuschel, on the growth and yield components of rice, Oryza sativa, were evaluated using four varieties of rice, ‘Cocodrie’, ‘Cypress’, ‘Bengal’ and ‘XP1003’, over 2 years. 2 Both adults and larvae of L. oryzophilus feed on rice plants, but it is feeding by the larval stage that causes economic losses. Feeding by L. oryzophilus larvae resulted in extensive damage to root systems. Pruning of root systems resulted in a decrease in tiller number and shoot biomass of rice plants in the vegetative stage of growth. 3 Yield losses were due to a combination of decreases in panicle densities, numbers of grains per panicle, and grain weights. Decreases in panicle densities were a direct result of the reductions in tiller numbers. Reductions in numbers of grains per panicle and grain weights probably resulted from decreases in shoot biomass. 4 Injury by rice water weevil larvae is chronic. The tillering stage of rice suffered the majority of weevil damage, but the growth effects were not manifested until later.     

Comparison of two populations of Pseudophilothrips ichini (Thysanoptera: Phlaeothripidae) as candidates for biological control of the invasive weed Schinus terebinthifolia (Sapindales: Anacardiaceae)

Brazilian peppertree, Schinus terebinthifolia Raddi (Sapindales: Anacardiaceae) (hereafter Schinus), is one of the worst invasive species in Florida and Hawaii. The thrips Pseudophilothrips ichini Hood (Thysanoptera: Phlaeothripidae) is being considered as a potential biological control agent of Schinus. Two populations of this thrips were collected in the weed's native range; one from central-east Brazil (Ouro Preto thrips) and a second from north-east Brazil (Salvador thrips). Temperature requirements, adult fecundity and impact on different plant haplotypes by P. ichini were examined in the laboratory. Complete development of thrips from both populations occurred at temperatures ranging from 20 to 30°C. Two approaches were used to model the predicted distributions of the thrips populations in the USA: the physiological model (NAPPFAST) based on cold tolerance and the ecological niche model based on climatic variables (MaxEnt). The physiological model predicted that both populations of P. ichini may establish in similar areas of the USA, overlapping with the distribution of Schinus. However, the niche model predicted that only the Ouro Preto thrips could establish in the USA. The difference in model predictions suggests an apparent preadaptation of the Salvador thrips to lower temperatures than those experienced at the locations they were collected in Brazil. The Ouro Preto thrips had similar fecundity on two Florida Schinus haplotypes, whereas lower fecundity on haplotype A was found for the Salvador thrips. Based on these results, the Ouro Preto population may be better adapted to the climatic conditions and plant haplotypes found in Florida. Moreover, greenhouse studies indicated that Schinus growth was greatly reduced by thrips feeding, which may result in lower weed reproduction and densities in the field.