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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

No evolution of increased competitive ability or decreased allocation to defense in <Emphasis Type="Italic">Melaleuca quinquenervia</Emphasis> since release from natural enemies

If invasive plants are released from natural enemies in their introduced range, they may evolve decreased allocation to defense and increased growth, as predicted by the evolution of increased competitive ability (EICA) hypothesis. A field experiment using the invasive tree Melaleuca quinquenervia was conducted to test this hypothesis. Seeds were collected from 120 maternal trees: 60 in Florida (introduced range) and 60 in Australia (home range). Plants grown from these seeds were either subjected to herbivory by two insects from Australia that have recently been released as biological control agents or protected from herbivores using insecticides. Genotypes from the introduced range were initially more attractive to herbivores than genotypes from the home range, supporting EICA. However, genotypes from the introduced and home range did not differ in resistance to insects or in competitive ability, which does not support EICA. Plants from the introduced range had a lower leaf hair density, lower leaf: stem mass ratio, and a higher ratio of nerolidol: viridifloral chemotypes compared to plants from the native range. Plants with an intermediate density of leaf hairs and with high specific leaf area were more susceptible to herbivory damage, but there were no effects of leaf toughness or chemotype on presence of and damage by insects. Herbivory had a negative impact on performance of Melaleuca. Other than an initial preference by insects for introduced genotypes, there was no evidence for the evolution of decreased defense or increased competitive ability, as predicted by the EICA hypothesis. It does not appear from this study that the EICA hypothesis explains patterns of recent trait evolution in Melaleuca.     

Herbivorous insects reduce growth and reproduction of big sagebrush (<Emphasis Type="Italic">Artemisia tridentata</Emphasis>)

Insect herbivores can reduce growth, seed production, and population dynamics of host plants, but do not always do so. Big sagebrush (Artemisia tridentata) has one of the largest ranges of any shrub in North America, and is the dominant and characteristic shrub of the extensive sagebrush steppe ecosystem of the western United States. Nevertheless, the impact of insect herbivores on big sagebrush, its dominant and characteristic shrub, is largely unknown. Occasional large effects of insect herbivore outbreaks are documented, but there is little knowledge of the impact of the more typical, nominal herbivory that is produced by the diverse community of insects associated with big sagebrush in natural communities. In 2008, we removed insects from big sagebrush plants with insecticide to evaluate whether insect herbivores reduced growth and seed production of big sagebrush. Removal of herbivores led to significant and substantial increases in inflorescence growth (22%), flower production (325%), and seed production (1053%) of big sagebrush. Our results showed the impact of insect herbivory in the current growing season on the growth and reproduction of big sagebrush and revealed an unrecognized, significant role of non-outbreak herbivores on big sagebrush.     

An experimental test of the evolution of increased competitive ability hypothesis in goldenrod, <Emphasis Type="Italic">Solidago gigantea</Emphasis>

The mechanisms that allow introduced plants to become invasive are poorly understood. Here, we present a test of the evolution of increased competitive ability hypothesis, which holds that because specialized natural enemies may be absent from the introduced range, exotic plants may evolve to invest less in anti-herbivore defenses and thereby gain a competitive advantage over native plants. We grew Solidago gigantea plants derived from both the native range (North America) and the invasive range (Europe) in a common garden in the native range for 2 years. Half the plants were treated with insecticide to protect them from insect herbivores and the other half were exposed to insects that colonized the garden from nearby fields. Insect herbivore biomass was significantly higher on European plants than US plants in the first year but not the second. European plants were more heavily attacked by pathogens in both years of the study. When exposed to insect herbivores, US plants produced more seed than European plants, but when plants were protected from herbivores, seed production was equivalent between US plants and European plants. The presence of insect herbivores suppressed seed production of European plants much more than that of US plants, even though the level of herbivory experienced by European and US plants was similar in the second year, suggesting that the ability to tolerate herbivory was diminished in European plants. These results partially support the EICA hypothesis: plants from the introduced range were more susceptible to some natural enemies and benefited more from insect removal than plants from the native range. The prediction that European plants would perform better than US plants in the absence of insect herbivores was not supported. Electronic Supplementary Material Supplementary material is available for this article at     

The influence of herbivory and weather on the vital rates of two closely related cactus species

Herbivory has long been recognized as a significant driver of plant population dynamics, yet its effects along environmental gradients are unclear. Understanding how weather modulates plant–insect interactions can be particularly important for predicting the consequences of exotic insect invasions, and an explicit consideration of weather may help explain why the impact can vary greatly across space and time. We surveyed two native prickly pear cactus species (genus Opuntia) in the Florida panhandle, USA, and their specialist insect herbivores (the invasive South American cactus moth, Cactoblastis cactorum, and three native insect species) for five years across six sites. We used generalized linear mixed models to assess the impact of herbivory and weather on plant relative growth rate (RGR) and sexual reproduction, and we used Fisher's exact test to estimate the impact of herbivory on survival. Weather variables (precipitation and temperature) were consistently significant predictors of vital rate variation for both cactus species, in contrast to the limited and varied impacts of insect herbivory. Weather only significantly influenced the impact of herbivory on Opuntia humifusa fruit production. The relationships of RGR and fruit production with precipitation suggest that precipitation serves as a cue in determining the trade‐off in the allocation of resources to growth or fruit production. The presence of the native bug explained vital rate variation for both cactus species, whereas the invasive moth explained variation only for O. stricta. Despite the inconsistent effect of herbivory across vital rates and cactus species, almost half of O. stricta plants declined in size, and the invasive insect negatively affected RGR and fruit production. Given that fruit production was strongly size‐dependent, this suggests that O. stricta populations at the locations surveyed are transitioning to a size distribution of predominantly smaller sizes and with reduced sexual reproduction potential.     

Temperature-dependent development and potential distribution of Episimus utilis (Lepidoptera: Tortricidae), a candidate biological control agent of Brazilian peppertree (Sapindales: Anacardiaceae) in Florida

The invasive Brazilian peppertree (Schinus terebinthifolius Raddi), native to South America, is widely established throughout central and south Florida. The defoliating leaflet-roller Episimus utilis Zimmerman was selected as potential biocontrol agent of this invasive species. The objectives of this study were to determine development rate and survival of E. utilis at seven constant temperatures (10, 15, 20, 25, 30, 33, and 35 degrees C) and generate prediction maps of the number of generations per year this species may exhibit in the United States. The rate of development of E. utilis as a function of temperature was modeled using linear regression to estimate a lower developmental threshold of 9.6 degrees C and the degree-day requirement of 588. The Logan nonlinear regression model was used to estimate an upper developmental threshold of 33 degrees C. Cold tolerance of E. utilis was examined using all insect stages, and each stage was exposed to three constant temperatures (10, 5, 0 degrees C) for 0.5, 1, 2, 4, and 8 d (or until all insects died). The pupal stage was the most cold tolerant with 100% mortality after 12 d at 0 degrees C. The pupal lethal times at 5 (Ltime50 = 10 d, Ltime90 = 28 d) and 0 degrees C (Ltime50 = 5 d, Ltime90 = 9 d) were used to generate isothermal lines to predict favorable regions for E. utilis establishment. A GIS map was generated to predict the number of generations of E. utilis (range, 0.5-9.8) across all Brazilian peppertree range in the United States. The potential for establishment of E. utilis and its probable distribution in the continental United States was examined.     

Do carbon-based defences reduce foliar damage? Habitat-related effects on tree seedling performance in a temperate rainforest of Chiloé Island, Chile

Carbon-based secondary compounds (CBSCs), such as phenols or tannins, have been considered as one of the most important and general chemical barriers of woody plants against a diverse array of herbivores. Herbivory has been described as a critical factor affecting the growth and survival of newly established tree seedlings or juveniles then, the presence of secondary metabolites as defences against herbivores should be a primary strategy to reduce foliar damage. We examined whether light-induced changes in leaf phenolic chemistry affected insect herbivory on seedlings of two rainforest tree species, Drimys winteri (Winteraceae) and Gevuina avellana (Proteaceae). Seedlings of both species were planted under closed canopy and in a canopy gap within a large remnant forest patch. Half of the seedlings in each habitat were disinfected with a wide-spectrum systemic insecticide and the other half were used as controls. Seedling growth, survival, and foliar damage (estimated by an herbivory index) due to insect herbivores were monitored over a period of 16 months (December 2001–April 2003). The total leaf content of phenols and condensed tannins were assessed in seedlings from both habitats. As expected, access to light induced a greater production of CBSCs in seedlings of both tree species, but these compounds did not seem to play a significant defensive role, as seedlings grown in gaps suffered greater leaf damage than those planted in forest interior. In addition, in both habitats, seedlings without insecticide treatment suffered a greater foliar damage than those with insecticide, especially 16 months after the beginning of the experiment. Canopy openness and herbivory had positive and negative effects, respectively, on seedling growth and survival in both tree species. In conclusion, despite the higher levels of defence in tree-fall gap, the higher densities of herbivore override this and lead to higher damage levels.     

Differential attack on diploid, tetraploid, and hexaploid Solidago altissima L. by five insect gallmakers

Genetic variation among plants can influence host choice and larval performance in insect herbivores. Ploidy (cytotype) variation is a particularly dramatic form of plant genetic variation, and where diploid and polyploid cytotypes of a species occur in sympatry, they may provide herbivores with choices that are distinguished by profound and genome-wide genetic differences. We tested for non-random attack by five gallmaking insect herbivores on diploid, tetraploid, and hexaploid cytotypes of the goldenrod Solidago altissima L., working in seven midwestern US populations where the ploidies co-occur on spatial scales relevant to insect host choice. For four of the five herbivores, attack was non-random with respect to ploidy at one or more sites. Ploidy effects on attack were complex: the ploidy subjected to highest attack varied both across herbivores within sites and (for most herbivores) across sites within herbivores. Ploidy effects on attack will alter rates of encounter between insect herbivores—either increasing or decreasing the likelihood of two herbivores sharing a host plant ramet, compared with the case with no effects of ploidy. Plant ploidy variation appears likely to have a major impact on insect community organization, and perhaps on plant–herbivore coevolution, but that impact is likely to be spatially heterogeneous. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.