James P. Cuda

Chloroplast and microsatellite DNA diversities reveal the introduction history of Brazilian peppertree (Schinus terebinthifolius) in Florida.

Brazilian peppertree (Schinus terebinthifolius) is a woody perennial that has invaded much of Florida. This native of northeastern Argentina, Paraguay, and Brazil was brought as an ornamental to both the west and east coasts of Florida at the end of the 19th century. It was recorded as an invader of natural areas in the 1950s, and has since extended its range to cover over 280 000 ha. Our goals were to understand the history of this invasion, as one step toward understanding why this exotic was so successful, and ultimately to improve development of biological control agents. We sampled plants from the native and exotic ranges, particularly Florida, and genotyped these individuals at nuclear and chloroplast loci. Nuclear microsatellite and cpDNA loci reveal strong genetic population structure consistent with limited dispersal in the introduced and native ranges. Bayesian clustering of microsatellite data separates the east and west coast plants in Florida into distinct populations. The two chloroplast haplotypes found in Florida are also concordant with this separation: one predominates on the east coast, the other on the west coast. Analysis of samples collected in South America shows that haplotypes as distinct as the two in Florida are unlikely to have come from a single source population. We conclude that the genetic evidence supports two introductions of Brazilian peppertree into Florida and extensive hybridization between them. The west coast genotype likely came from coastal Brazil at about 27° south, whereas the east coast genotype probably originated from another, as yet unidentified site. As a result of hybridization, the Florida population does not exhibit low genetic variation compared to populations in the native range, possibly increasing its ability to adapt to novel environments. Hybridization also has important consequences for the selection of biocontrol agents since it will not be possible to identify closely co‐adapted natural enemies in the native range, necessitating more extensive host testing.

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.

Brazilian peppertree (Schinus terebinthifolius) in Florida and South America: evidence of a possible niche shift driven by hybridization

Brazilian peppertree (Schinus terebinthifolius Raddi, Anacardiaceae) was introduced into Florida from South America in the 1800s and commercialized as an ornamental plant. Based on herbaria records and available literature, it began to escape cultivation and invade ruderal and natural habitats in the 1950s, and is now considered to be one of Florida’s most widespread and damaging invasive plants. Historical records and molecular evidence indicate that two genetic lineages of Brazilian peppertree were established in Florida, one in Miami on the east coast and a second near Punta Gorda on the west coast. Since arriving, the distributions of these two types have greatly expanded, and they have extensively hybridized. Principal component analysis and reciprocal niche fitting were used to test the equivalency of climatic niches of the Florida populations with the climatic niches of the two South American chloroplast haplotype groups which established in Florida. Both approaches indicated a significant shift in niches between the parental populations in the native range and the invasive populations in Florida. The models, however, closely predicted the areas of initial establishment. We hypothesize that (1) Brazilian peppertree was able to gain an initial foothold in Florida due to niche similarity and (2) the current dissimilarity in native and exotic niches is due to hybridization followed by rapid selection of genotypes adapted to Florida’s climate. In addition, to examine the potential consequence of the introduction of additional genetic diversity from the native range on invasion success, a niche model constructed with occurrences of all native genotypes was projected onto the continental United States. The result of this test indicated that under such an event, the potential invasive range would greatly expand to cover most of the southeastern USA. Our study suggests that multiple introductions from disjunct regions in the native range can facilitate invasion success.

Natural Enemies of Brazilian Peppertree (Sapindales: Anacardiaceae) from Argentina: Their Possible Use for Biological Control in the USA

ABSTRACT Brazilian peppertree (Schinus terebinthifolius Raddi, Anacardiaceae) is a perennial tree native to Argentina, Brazil, and Paraguay. The plant was introduced into the USA before 1900. Originally grown as an ornamental, Brazilian peppertree is now considered an noxious plant in Hawaii and Florida, where it is ranked among the most important threats to biodiversity in natural areas. Recent surveys conducted in northeastern Argentina recovered one fungus associated with distorted leaves and 36 phytophagous insects collected on Brazilian peppertree. A leaf-feeding notodontid moth, a new species of gracillariid leaf blotch miner, and a stem-boring weevil have been selected for further studies to determine their potential as biological control agents of Brazilian peppertree in the USA. The results of these surveys are summarized herein and descriptions are included of the insects that are considered most promising for biological control of this weed.

Gratiana boliviana, a potential biocontrol agent of Solanum viarum: Quarantine host-specificity testing in Florida and field surveys in South America

Host-specificity tests andfield surveys were conducted to determine thesuitability of the tortoise beetleGratiana boliviana Spaeth (Coleoptera:Chrysomelidae) from Argentina for classicalbiological control of Solanum viarumDunal (Solanaceae) in the USA. Thehost-specificity tests were conducted at theFlorida Department of Agriculture and ConsumerServices-Division of Plant Industry quarantinefacility in Gainesville, Florida (USA). Multiple-choice host-specificity tests wereconducted in small cages using 123 plantspecies in 35 families. Adults fedsignificantly (>41% of the leaf area offeredwas damaged) on the target weed(S. viarum), and fed lightly (<20%) onSolanum torvum Sw. (noxious weed native towest-Africa). Adults did some exploratoryfeeding (<5%) on eggplant, Solanummelongena L. (economic crop), Solanumelaeagnifolium Cav. (major agricultural weedin the western US), and on Solanumtampicense Dunal (weed of Central Americanorigin). No feeding was observed on any of theother 118 plant species that were testedincluding another 21 Solanum species.G. boliviana adults laid an average of 68eggs per female on S. viarum, 5 eggs perfemale on S. torvum, and an average of0.2 eggs on eggplant. No-choicehost-specificity tests were also conducted inwhich G. boliviana adults and neonatelarvae were exposed to 19 and 22 plant speciesrespectively. Tests with the neonatesindicated this insect was able to complete itsdevelopment only on S. viarum (67%reached the pupae stage). The no-choice testswith adults indicated that this insect fed,laid eggs, and completed development only onS. viarum. The unsprayed eggplant fieldsthat were surveyed in its natural range inArgentina, Brazil, Paraguay, and Uruguay fromJune 1997 to March 2000 indicated thatG. boliviana is not a pest of eggplants in SouthAmerica. Therefore, a petition for fieldrelease of G. boliviana for classicalbiological control of S. viarum in theUSA was submitted in April 2000.

Biology and Laboratory Rearing of Cricotopus lebetis (Diptera: Chironomidae), a Natural Enemy of the Aquatic Weed Hydrilla (Hydrocharitaceae)

Abstract Field and laboratory studies were conducted on Cricotopus lebetis Sublette, a midge of unknown origin that causes widespread damage to the aquatic weed hydrilla, Hydrilla verticillata (L.f.) Royle, at Crystal River, FL, USA. The larvae of C. lebetis burrow into the submersed apical meristems of the hydrilla plant and destroy shoot tips during their development. Abscission of the hydrilla stem tip usually occurs when the last instar excavates a tunnel inside the stem for pupation. Mining damage caused by the feeding larvae induces stunting and basal branching that alters the normal growth pattern of hydrilla. Larval populations of C. lebetis and damaged hydrilla shoot tips were highest in the summer (May and June) and fall months (October and November) during 1997 and 1998. In June 1998, more than 70% of the hydrilla shoot tips were damaged by midge larvae. Adults lived <2 d in the laboratory, and nuptial flights were not a prerequisite for mating. Females deposited a single egg string containing an average of 154 eggs inside a gelatinous matrix. The eggs took ≈2 d to complete development and neonate eclosion was synchronized. The larval stage had four instars and required ≈14 d to develop to the pupal stage, which lasted an additional 2 d. Although most larval chironomids feed on algae or detritus, the larvae of C. lebetis fed and developed entirely on the living stem tissue of hydrilla.

OPEN-FIELD HOST SPECIFICITY TEST OF GRATIANA BOLIVIANA (COLEOPTERA: CHRYSOMELIDAE), A BIOLOGICAL CONTROL AGENT OF TROPICAL SODA APPLE (SOLANACEAE) IN THE UNITED STATES

Abstract An open-field experiment was conducted to assess the suitability of the South American leaf feeding beetle Gratiana boliviana Spaeth for biological control of Solanum viarum Dunal in the USA. An open-field test with eggplant, Solanum melongena L., was conducted on the campus of the University of Buenos Aires, Argentina, and a S. viarum control plot was established 40 km from the campus. One hundred adult beetles were released in each plot at the beginning of the experiment during the vegetative stage of the plants, and forty additional beetles were released in the S. melongena plot at the flowering stage. All the plants in each plot were checked twice a week and the number of adults, immatures, and eggs recorded. Results showed almost a complete rejection of eggplant by G. boliviana. No noticeable feeding damage was ever recorded on eggplant. The experiment was ended when the eggplants started to senesce or were severely damaged by whiteflies and spider mites. The results of this open-field experiment corroborate previous quarantine/laboratory host-specificity tests indicating that a host range expansion of G. boliviana to include eggplant is highly unlikely. Gratiana boliviana was approved for field release in May 2003 in the USA. To date, no non-target effects have been observed either on eggplant or native species of Solanum.

Biology and Laboratory Rearing of Episimus utilis (Lepidoptera: Tortricidae), a Candidate for Classical Biological Control of Brazilian Peppertree (Anacardiaceae) in Florida

Abstract The biology of Episimus utilis Zimmerman, a natural enemy of Brazilian peppertree, Schinus terebinthifolius Raddi, was investigated in a quarantine laboratory as part of a classical biological control program against this invasive weed in Florida. Adults lived on average 6.8 ± 0.8 d, and a generation was completed in 43.6 d at a temperature of 22.0°C and a photoperiod of 12:12 (L:D) h. Peak egg production occurred 2 d after females eclosed from the pupal stage. Females deposited a maximum of 172 eggs, with an average daily maximum of 13.6 eggs. The durations of the egg, larval, and pupal stages were 5.9, 23.7 (five instars), and 12.0 d, respectively. Stage-specific life tables were constructed to calculate basic population statistics. Under laboratory conditions where predation and food supply were not limiting factors, a population of E. utilis was capable of multiplying its population by 1.17 times per day, and a doubling of the population would occur every 4.4 d. To date, 10 consecutive generations of E. utilis have been produced on potted Brazil peppertree plants in the laboratory. The potential effectiveness of E. utilis as a biological control agent of Brazilian peppertree in Florida was examined using Goeden’s revision of the Harris scoring system.

Temperature-dependent development, survival, and potential distribution of Ischnodemus variegatus (Hemiptera: Blissidae), a herbivore of West Indian marsh grass.

Abstract The bug Ischnodemus variegatus (Signoret) (Hemiptera: Blissidae) is an adventive herbivore, native to South America that feeds in the invasive grass Hymenachne amplexicaulis (Rudge) Nees (Poaceae). This grass is a problematic weed in Florida and Australia, but it is a highly valued forage in Mexico, Cuba, and Venezuela. We studied the influence of nine constant temperatures (8–38°C) on the developmental time and survival of I. variegatus. Complete egg and nymphal mortality occurred at temperatures ≤20.5°C and at 38°C. Developmental time decreased linearly with temperature until 28–30°C and then increased at 33°C. Mortality of first, second, and third instars was high across all temperatures. Developmental time across all temperatures was greatest for eggs, first and fifth instars compared with other stages. Linear and Brière-1 nonlinear models were used to determine the lower temperature threshold at which the developmental rate (1/D) approached zero. The lower thresholds to complete development (egg to adult) estimated with the linear and nonlinear model were 14.6 and 17.4°C, respectively. The total degree-days required to complete development estimated by the linear model was 588. Using temperature data from Florida, a map was generated to project a prediction grid of I. variegatus generations per yr. Based on these predictions, the insect can complete three to five generations per year in areas currently invaded in Florida. Results of this study will be used to understand the potential distribution and population growth of I. variegatus in H. amplexicaulis infested regions.

Fundamental host range of Pseudophilothrips ichini s.l. (Thysanoptera: Phlaeothripidae): a candidate biological control agent of Schinus terebinthifolius (Sapindales: Anacardiaceae) in the United States.

ABSTRACT Schinus terebinthifolius Raddi (Sapindales: Anacardiaceae) is a non-native perennial woody plant that is one of the most invasive weeds in Florida, Hawaii, and more recently California and Texas. This plant was introduced into Florida from South America as a landscape ornamental in the late 19th century, eventually escaped cultivation, and now dominates entire ecosystems in south-central Florida. Recent DNA studies have confirmed two separate introductions of S. terebinthifolius in Florida, and there is evidence of hybridization. A thrips, Pseudophifothrips ichini s.l. (Hood) (Thysanoptera: Phlaeothripidae), is commonly found attacking shoots and flowers of S. terebinthifolius in Brazil. Immatures and occasionally adults form large aggregations on young terminal growth (stems and leaves) of the plant. Feeding damage by P. ichini s.l. frequently kills new shoots, which reduces vigor and restricts growth of S. terebinthifolius. Greenhouse and laboratory host range tests with 46 plant species in 18 families and 10 orders were conducted in Parana, Brazil, and Florida. Results of no-choice, paired-choice, and multiple-choice tests indicated that P. ichini s.l. is capable of reproducing only on S. terebinthifolius and possibly Schinus molle L., an ornamental introduced into California from Peru that has escaped cultivation and is considered invasive. Our results showed that P. ichini s.l. posed minimal risk to mature S. molle plants or the Florida native Metopium toxiferum L. Krug and Urb. In May 2007, the federal interagency Technical Advisory Group for Biological Control Agents of Weeds (TAG) concluded P. ichini s.l. was sufficiently host specific to recommend its release from quarantine.