BioControl (2009) 54:475–484 DOI 10.1007/s10526-008-9196-3

Influence of host-plant quality on the performance of Episimus unguiculus, a candidate biological control agent of Brazilian peppertree in Florida

Veronica Manrique Æ J. P. Cuda Æ W. A. Overholt Æ S. M. L. Ewe

Received: 18 June 2008 / Accepted: 30 October 2008 / Published online: 15 November 2008 Ó International Organization for Biological Control (IOBC) 2008

Abstract Brazilian peppertree, Schinus terebinthifo- addition, higher survival (40%), faster development lius Raddi (Sapindales: Anacardiaceae), introduced (34 day) and higher fertility (88% eggs hatched) from South America, invades a variety of habitats in occurred in high-nutrient treatments. Based on these Florida (e.g. disturbed sites, coastal mangrove forests). results, field releases should be conducted in favorable The objective of this study was to evaluate the effect of habitats (e.g., low salinity, high fertility soils) to host-plant quality on the performance of Episimus maximize the possibility of establishment and popu- unguiculus Clarke (=E. utilis Zimmerman) (Lepidop- lation growth of E. unguiculus in Florida. tera: ), a potential biocontrol agent of Brazilian peppertree. Experiments were conducted in Keywords –plant interactions Á the laboratory using Brazilian peppertrees exposed Weed biological control Á Tortricidae Á either to different salinity levels (0, 6, 12 parts per Anacardiaceae Á Schinus terebinthifolius 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 Introduction

Brazilian peppertree, Schinus terebinthifolius Raddi Handling Editor: John Scott. (Sapindales: Anacardiaceae), is an introduced peren- nial plant that has become widely established & V. Manrique ( ) Á W. A. Overholt throughout central and south Florida (Cuda et al. Biological Control Research and Containment Laboratory, University of Florida, 2199 South Rock Road, 2006). This species is native to Argentina, Brazil and Fort Pierce, FL 34945, USA Paraguay (Barkley 1944, 1957), and was brought to e-mail: vero72@ufl.edu Florida as an ornamental in the 1840s (Mack 1991). Brazilian peppertree not only colonizes disturbed J. P. Cuda Department of Entomology and Nematology, University sites such as highway right-of-way, canals, fallow of Florida, Bldg. 970 Natural Area Drive, Gainesville, farmlands, and drained wetlands, but also invades FL 32611, USA natural communities, including pinelands, hardwood hammocks and mangrove forests in Florida (Myrtin- S. M. L. Ewe Ecology and Environment, Inc., 1665 Palm Beach Lakes ger and Williamson 1986; Ewe 2001; Cuda et al. Blvd., West Palm Beach, FL 33401, USA 2006). The invasion and displacement of native 123 476 V. Manrique et al. species by Brazilian peppertree poses a serious threat leaflets together to feed, whereas older instars feed to biodiversity in many ecosystems of Florida and pupate inside a cylindrical rolled leaflet. The (Morton 1978). Several attributes of this plant dimorphic adults are small, grayish brown with distinct contribute to its invasiveness, including a large wing patterns that separate the sexes (Zimmerman number of fruits produced per female plant, an 1978). Because the entire life cycle of E. unguiculus effective mechanism of dispersal by birds (Panetta occurs in the canopy of the host plant, this insect may be and McKee 1997), tolerance to shade (Ewel 1979), well adapted to areas subjected to seasonal flooding in fire (Doren et al. 1991), and drought (Nilson and south Florida. Host-specificity studies conducted in Muller 1980b), allelopathic effects on neighboring Brazil and Florida quarantine showed that larval plants (Gogue et al. 1974; Nilson and Muller 1980a; feeding damage was restricted to plants in the family Morgan and Overholt 2006), and tolerance to saline Anacardiaceae in no-choice tests, and Brazilian conditions (Ewe 2001; Ewe and Sternberg 2002). peppertree was the preferred host in choice tests Although herbicides and mechanical methods (J. P. Cuda, unpublished data). A petition for the (e.g., cutting, burning and flooding) are routinely release E. unguiculus in Florida for biological control of used for controlling existing Brazilian peppertree Brazilian peppertree is currently in preparation. stands (Gioeli and Langeland 2006; Cuda et al. 2006), Several factors influence the establishment of these methods are extremely labor intensive and can biological control agents, such as climate, natural be very expensive, especially for large infestations. In enemies present in the introduced range and host-plant addition, chemical and mechanical controls are quality (Sutherst and Maywald 1985; Wheeler and unsuitable for some natural areas (e.g., mangrove Center 1996; Hunter 2001; Wheeler 2001; Byrne et al. forests) because they may have negative effects on 2003; Senaratne et al. 2006). Furthermore, the nutri- non-target species (Doren and Jones 1997) and tional status of many weeds has played an important may increase water pollution. Therefore, alternative role in successful biological control programs (Myers methods for long-term control of Brazilian peppertree 1987; Julien and Griffiths 1998). For example, initial are urgently needed. A classical biological control applications of nitrogen fertilizer helped in the program was initiated in the 1980s, and the leaflet- establishment of Cactoblastis cactorum (Berg) roller Episimus unguiculus Clarke (: (Lepidoptera: Pyralidae) on prickly pear (Opuntia Tortricidae) was selected as a potential biocontrol spp.) cactus (Dodd 1940)andtheCyrtobagous salvinia agent of Brazilian peppertree because it clearly Calder and Sands (Coleoptera: Curculionidae) on damaged the plant and appeared to be host specific Salvinia molesta Mitchell (Salviniaceae) (Thomas and in its native range (Martin et al. 2004;Cudaetal. Room 1986). In addition, plant palatability varies 2006). Previous studies on this insect were published across salinity gradients (Levine et al. 1998;Moonand under the junior synonym Episimus utilis Zimmerman Stiling 2000;GoransonandHo2004), and high salinity (Razowski and Brown 2008). In the 1950s, E. ungui- levels may be detrimental to some insect herbivores culus was released and established in Hawaii, but (Hemminga and van Soelen 1988; Moon and Stiling successful control of Brazilian peppertree populations 2002; Schile and Mopper 2006). was not achieved (Goeden 1977; Yoshioka and Markin Because Brazilian peppertree invades different 1991; Julien and Griffiths 1998). However, its inability habitats in Florida (e.g., mangrove forests, pinelands, to control the plant in Hawaii should not preclude its abandoned farms), the environmental conditions release into other areas infested with Brazilian pepper- encountered in different habitats may influence the tree. Unfavorable abiotic or biotic factors may have survival and effectiveness of potential biocontrol contributed to its failure in Hawaii. For example, high agents. Therefore, the objective of this study was to larval mortality of E. unguiculus by introduced and evaluate the performance of E. unguiculus reared on native parasitoids and predators of agricultural pests Brazilian peppertree exposed to different salinity and was documented following its release (Davis 1959; nutrient levels in the laboratory. Results from this Krauss 1963). study will provide a better understanding of the The larvae of E. unguiculus feed on Brazilian interaction between Brazilian peppertree and peppertree leaflets and can completely defoliate small E. unguiculus, one of its principal herbivores. This plants (Martin et al. 2004). Early instars tie young information will improve the selection of release sites 123 Influence of host-plant quality on Episimus unguiculus performance 477 favorable for establishing the insect in Florida (ppt)), (2) low saline environment (6 ppt salinity), following its release from quarantine. and (3) high saline environment (12 ppt salinity). Brazilian peppertree plants were either irrigated with tap water (fresh water environment) or with water Materials and methods supplemented with seawater (36 ppt) to obtain 6 or 12 ppt salinity. In order to prevent plant stress, a Insect rearing stepwise increase in salt concentration (1 ppt every three days) was used. Plants were irrigated with each Laboratory experiments were conducted at the Bio- salinity level for the duration of the experiment logical Control Research and Containment Laboratory (*two months). Brazilian peppertree invades (BCRCL) located at the Indian River Research different habitats in Florida, including transitional and Education Center (IRREC) of the University of mangrove forests where salinity levels range between Florida, Fort Pierce, FL, USA. A colony of 0 and 25 ppt depending on the time of the year (rainy E. unguiculus was initiated in August of 2006 at the vs. dry season) (Ewe 2001). Thus, the salinity levels BCRCL, and were reared on individual used in this study (6 and 12 ppt) are within the range Brazilian peppertree plants (Florida genotypes) grown of values encountered in the field. in nursery pots (18 cm height, 17 cm diameter) inside Several plant parameters were recorded at the environmental growth chambers (25 ± 2°C, 60–70% beginning of the experiment (four to six replicates RH, 14L: 10D photoperiod) (see Martin et al. (2004) per treatment): (1) leaflet toughness (g mm-2), (2) for rearing procedures). Insects were originally specific leaflet area (SLA = leaf area/leaf dry collected in 2003 in the vicinity of Curitiba located weight), (3) percent leaflet moisture content (LMC = in the Parana Province of southern Brazil, and (fresh - dried leaf weight) 9 100/fresh weight), and imported to the quarantine facility in Gainesville, (4) leaflet nutrient (N, P, K) and sodium contents FL. Voucher specimens of E. unguiculus were depo- (Na). Leaflet toughness was measured using a sited in the Florida State Collection of , modified 300 g Pesola scale (Forestry Suppliers Florida Department of Agriculture and Consumer Inc., Jackson, MS) with a probe that estimates the Services, Gainesville, Florida, USA. pressure required to puncture leaflet tissues (average of four punctures per leaflet). Leaflet toughness, SLA Plants used in experiments and LMC were determined for one newly expanded leaflet (second from top of the stem), and one mature Brazilian peppertree plants were grown from seeds leaflet (third from bottom of the stem) from each collected from a saline environment in Florida’s east treatment plant. The leaflets were scanned into the coast (Fort Pierce, FL) to assure plant adaptability to computer and Image-J (ImageJ NIH) software was those conditions. Plants were maintained in a green- used to measure leaf areas. For the nutrient and Na house in nursery pots (18 cm height, 17 cm diameter analyses, leaflet samples from each plant were pots) containing a mixture of soil (FafardÒ #3B mix) harvested, oven-dried at 70°C for one week and and sand (1:1). Plants were fertilized monthly with ground; all samples were sent to the Agricultural 400 ml per pot of liquid fertilizer (Miracle GrowÒ Analytical Services Laboratory, Pennsylvania State 24-8-16) and watered as needed. Four-months old University, PA, USA. plants were assigned randomly to the different Experiments were conducted inside an environ- treatments described below. mental growth chamber (25 ± 2°C, 60–70% RH, 14L: 10D photoperiod) starting on December 15, Performance of E. unguiculus on Brazilian 2006. Ten neonate larvae of E. unguiculus were peppertree exposed to different salinity levels caged on each potted plant inside a clear acrylic cylinder (45 cm height, 15 cm diameter) with six Forty-five days prior to initiating the experiments, holes (6 cm diameter) and tops covered by a fine three levels of soil salinity were established on the mesh to allow air circulation. After 15 days, plant test plants as follows (eight replicates each): (1) fresh foliage was carefully examined and removed; mature water environment (0 parts per thousand salinity larvae were placed individually inside plastic vials 123 478 V. Manrique et al.

(29.57 ml, Bio-Serv, Frenchtown, NJ) containing parameters were recorded as in the salinity study: moist filter paper and one plant leaflet to facilitate (1) pupal weight (mg), (2) developmental time from pupation and adult emergence. Time of development neonate to adult (days), (3) survival to adulthood (%), of E. unguiculus from first instar to pupal stage is (4) adult longevity (days), (5) fecundity (total eggs completed in 20 days at 25°C (Manrique et al. 2008), laid), and (6) fertility (% eggs hatched). but the experiment was ended before pupation to allow individual measurements of insect develop- Data analyses ment. To measure oviposition, newly emerged adult pairs from each treatment (4–5 pairs per treatment) Insect parameters (% survival to adult, adult lon- were placed inside wax paper cages (rectangles of gevity, fecundity, and fertility) and plant parameters 19 9 30 cm) containing one Brazilian peppertree (leaflet toughness, SLA, LMC, and nutrient content) leaflet and a cotton wick with GatoradeÒ for food were compared among treatments (different salinity (Moeri 2007). The oviposition cages were placed levels or nutrient levels) using one-way analysis inside ZiplocÒ freezer plastic bags and kept in the of variances (ANOVA) (SAS Institute 1999). The environmental growth chamber (same as before). proportion of individuals surviving and the pro- After all adults had died, the numbers of hatched and portion of eggs hatched were arcsine-square-root unhatched eggs were counted using a microscope. transformed prior to analysis (Zar 1999). Pupal Several insect parameters were recorded: (1) pupal weight was compared between treatments and gender weight (mg), (2) developmental time from neonate to using two-way ANOVA (SAS Institute 1999). Means adult (days), (3) survival to adulthood (%), (4) adult were separated using the post-hoc Student–Neuman– longevity (days), (5) fecundity (total eggs laid), and Keuls (SNK) test (SAS Institute 1999). A significance (6) fertility (% eggs hatched). level of a = 0.05 was used for all statistical analyses. Performance of E. unguiculus on Brazilian peppertree exposed to different nutrient levels Results Two months before initiating the experiment, three nutrient levels were established on the test plants as Performance of E. unguiculus on Brazilian follows (eight replicates each): (1) low nutrient-level peppertree exposed to different salinity levels (no fertilizer), (2) medium nutrient-level (fertilized once per month using 4 mg of fertilizer (Miracle Higher survival to the adult stage was obtained when GrowÒ 24-8-16) per liter of water), and (3) high insects were exposed to Brazilian peppertree plants nutrient-level (fertilized twice per month using grown in fresh-water (55%) and low salinity- Miracle GrowÒ 24-8-16). environments (36%), while survival was significantly Experiments were conducted inside an environ- lower under high salinity conditions (6%) (Table 1). mental growth chamber (25 ± 2°C, 60–70% RH, Duration of development to adulthood also differed 14L: 10D photoperiod) starting on August 15, 2007. between treatments with the longest time (44 days) Several plant parameters described previously were observed for larvae reared at the highest salinity level recorded at the beginning of the experiment (six to (12 ppt) (Table 1). However, adult longevity was eight replicates per treatment): (1) leaflet toughness, similar between treatments (Table 1). In addition, (2) SLA, and (3) LMC, and (4) leaflet nutrient (N, P, pupal weight differed significantly between treat- K) and Na contents. Ten neonate larvae of ments and adult gender, but the interaction was not E. unguiculus were caged on each potted plant inside significant (treatment: F1,28 = 45.11, P \ 0.0001; a clear acrylic cylinder. After 15 days, plant foliage gender: F1,28 = 4.92, P = 0.03; treatment 9 gender: was removed and examined for insects; mature larvae F1,28 = 0.03, P = 0.85). Higher pupal weight was were placed individually inside plastic vials obtained for E. unguiculus reared on Brazilian (29.57 ml, Bio-ServÒ, Frenchtown, NJ) containing peppertree plants grown in the fresh-water environ- moist filter paper and one plant leaflet to facilitate ment (18.93 ± 0.9 mg) (mean ± SE) compared to pupation and adult emergence. The same insect low salinity-environments (13.73 ± 1 mg), and 123 Influence of host-plant quality on Episimus unguiculus performance 479 female pupae (17.58 ± 0.9 mg) were significantly fresh-water environments compared to saline envi- heavier than males (15.68 ± 0.8 mg). However, no ronments, whereas significantly higher K and Na differences were detected in fecundity or fertility levels were recorded from low and high-saline between fresh and low saline environments (Table 1). environments (Table 2). In addition, toughness of Pupal weight and reproductive parameters were not mature leaflets (ML) was greater in the high-salinity examined for E. unguiculus reared under high- treatments (12 ppt), whereas specific leaflet area salinity conditions (12 ppt) due to low numbers of (SLA) of new expanded leaflets (NEL) was greater pupae and adults obtained. in the fresh-water treatment (Table 3). Percent leaflet Leaflet nutrient and Na contents also differed moisture content (LMC) in both NEL and ML was significantly between salinity treatments (Table 2). significantly higher in the fresh-water compared to Higher N and P values were obtained on leaflets from saline treatments (Table 3).

Table 1 Life history parameters of E. unguiculus (means ± SE) reared on Brazilian peppertree exposed to different salinity levels Salinity levels Survival to Time of development Adult longevity Fecundity (total Fertility adult (%) (days) (days) number eggs) (% egg hatched)

0 ppt 55.0 ± 8.9 a 32.3 ± 0.8 c 8.5 ± 0.6 91.2 ± 30.8 81.1 ± 5.3 6 ppt 36.2 ± 6.2 a 39.4 ± 1.0 b 8.9 ± 0.6 86.6 ± 6.9 81.6 ± 7.5 12 ppt 6.2 ± 3.2 b 44.4 ± 2.3 a 8.7 ± 0.9 – – F 18.6 24.2 0.2 0.03 0.03 df 2,23 2,19 2,15 1,8 1,8 P \0.0001 \0.0001 0.8 0.9 0.8 Different letters in the same column indicate statistical differences between treatments (P \ 0.05)

Table 2 Leaflet nutrient contents (means ± SE) of Brazilian peppertree exposed to different salinity levels Salinity levels N (%) P (%) K (%) Na (ug.g-1)

0 ppt 2.2 ± 0.07 a 0.4 ± 0.07 1.7 ± 0.19 b 4700.0 ± 465 b 6 ppt 1.8 ± 0.09 b 0.2 ± 0.01 2.7 ± 0.02 a 10906.0 ± 1185 a 12 ppt 1.8 ± 0.09 b 0.2 ± 0.006 2.9 ± 0.11 a 12452.0 ± 923 a F 6.07 3.9 18.7 28.1 P 0.01 0.05 0.0003 \0.0001 Different letters in the same column indicate statistical differences between treatments (P \ 0.05), df = 2,13

Table 3 Plant parameters (means ± SE) of Brazilian peppertree exposed to different salinity levels Salinity levels Leaflet toughness (g mm-2) Specific leaflet area (cm2 g-1) Leaflet moisture content (%) NEL ML NEL ML NEL ML

0 ppt 11.1 ± 1.4 24.6 ± 2.3 b 135.4 ± 6.5 a 100.3 ± 8.3 75.0 ± 4.6 a 67.2 ± 0.5 a 6 ppt 18.4 ± 3.2 30.8 ± 3.2 b 97.6 ± 11.2 b 84.1 ± 7.7 53.5 ± 3.2 b 56.2 ± 1c 12 ppt 25.0 ± 4.9 38.9 ± 1.6 a 86.0 ± 7.1 b 88.5 ± 8.6 52.8 ± 4.2 b 59.1 ± 0.9 b F 3.9 8.45 9.01 1.03 9.7 45.6 P 0.06 0.008 0.007 0.39 0.005 \0.0001 NEL new expanded leaflet, ML mature leaflet. Different letters in the same column indicate statistical differences between salinity treatments (P \ 0.05), df = 2,11 123 480 V. Manrique et al.

Performance of E. unguiculus on Brazilian of Na were detected in Brazilian peppertree leaflets peppertree exposed to different nutrient levels exposed to high nutrient treatment compared to the medium or low treatments (Table 5), confirming that Higher percent survival of E. unguiculus to the adult the application of fertilizer resulted in nutritional stage occurred on Brazilian peppertree plants exposed differences in leaves. In addition, lower toughness of to medium (25%) and high (40%) nutrient levels new expanded leaflets and higher leaflet moisture compared to the low level (1%) (Table 4). Time of content of mature leaflets were recorded on high development to the adult stage and adult longevity was nutrient plants compared to medium or low treat- similar on medium and high nutrient treatments ments (Table 6). Specific leaflet area (SLA) was not (Table 4). Although pupal weight did not differ influenced by nutrient treatments (Table 6). between medium and high nutrient treatments, female pupae (17.9 ± 0.5 mg) weighed more than male pupae

(16.36 ± 1.0 mg) (treatment: F1,19 = 0.42, P = 0.52; Discussion gender: F1,19 = 5.93, P = 0.02; treatment 9 gender: F1,19 = 0.00, P = 0.96). No differences were detected This study showed that the performance of the in fecundity of E. unguiculus females reared on candidate biocontrol agent E. unguiculus was influ- Brazilian peppertree plants grown in the medium or enced by its host-plant quality. Survival to the adult high nutrient treatments, whereas higher fertility (89% stage was similar when insects were reared either on eggs hatched) was obtained in the high nutrient Brazilian peppertree irrigated with freshwater (55%) treatment (Table 4). Development and reproductive or low-salinity environments (36%), whereas lower parameters were not examined for E. unguiculus reared survival was obtained for in the high-salinity envi- under low nutrient conditions due to low numbers of ronment (6%). In addition to high mortality, duration adults obtained. of development to adulthood for E. unguiculus was The leaflet nutrient contents likewise differed longest in the high-salinity environment, which between fertilization treatments (Table 5). Signifi- indicates poor host-quality for these plants. Thus, cantly higher levels of N, P, and K and lower levels insect herbivores that tolerate high-salinity levels

Table 4 Life history parameters of E. unguiculus (means ± SE) reared on Brazilian peppertree exposed to different nutrient levels Nutrient Survival to adult Time of development Adult longevity Fecundity (total number Fertility (% egg levels (%) (days) (days) eggs) hatched)

Low 1.2 ± 1.2 b – – – – Medium 25.0 ± 8.2 a 35.8 ± 1.1 11.9 ± 0.5 119.5 ± 16.5 78.9 ± 3.0 b High 40.0 ± 6.5 a 34.1 ± 0.8 11.3 ± 0.5 148.0 ± 21.7 88.7 ± 1.1 a F 12.8 1.6 0.9 1.1 6.2 df 2,2 1,12 1,11 1,9 1,9 P 0.0002 0.2 0.3 0.3 0.03 Different letters in the same column indicate statistical differences between treatments (P \ 0.05)

Table 5 Leaflet nutrient contents (means ± SE) of Brazilian peppertree exposed to different nutrient levels Nutrient levels N (%) P (%) K (%) Na (ug.g-1)

Low 0.9 ± 0.06 c 0.1 ± 0.01 c 1.9 ± 0.05 b 6233.3 ± 312.2 a Medium 1.5 ± 0.06 b 0.3 ± 0.02 b 1.7 ± 0.07 c 5939.2 ± 467.6 a High 2.0 ± 0.05 a 0.4 ± 0.02 a 2.2 ± 0.05 a 4712.8 ± 205.8 b F 77.1 50.4 20.33 5.44 P \0.0001 \0.0001 \0.0001 0.01 Different letters in the same column indicate statistical differences between treatments (P \ 0.05), df = 2,17 123 Influence of host-plant quality on Episimus unguiculus performance 481

Table 6 Plant parameters (means ± SE) of Brazilian peppertree exposed to different nutrient levels Nutrient levels Leaflet toughness (g) Specific leaflet area (cm2 g-1) Leaflet moisture content (%) NEL ML NEL ML NEL ML

Low 13.2 ± 1.4 a 28.1 ± 1.9 145.0 ± 14.6 124.5 ± 6.8 66.2 ± 1.5 67.2 ± 1.1 b Medium 9.5 ± 1.3 ab 28.9 ± 1.1 145.6 ± 9.1 132.6 ± 14.2 69.1 ± 1.2 70.1 ± 0.9 a High 7.4 ± 1.0 b 28.4 ± 1.7 169.8 ± 7.5 130.7 ± 10.4 70.0 ± 0.5 70.9 ± 0.7 a F 5.25 0.07 1.7 0.15 2.77 4.31 P 0.01 0.93 0.21 0.86 0.08 0.03 NEL new expanded leaflet, ML mature leaflet. Different letters in the same column indicate statistical differences between treatments (P \ 0.05), df = 2,23 should be identified for managing Brazilian pepper- (Slansky and Feeny 1977; Wheeler and Center 1996; tree stands growing in coastal areas with salinity Bowdish and Stiling 1998; Hinz and Muller-Scharer levels above 6 ppt. Differences in insect performance 2000; Stiling and Moon 2005). In contrast, large were also detected on Brazilian peppertree plants amounts of Na may disrupt metabolic function and exposed to different nutrient levels. Increased sur- could be detrimental to some insect herbivores vival of E. unguiculus was observed under medium (Wang et al. 2001; Wang 2002; Schile and Mopper (25%) and high (40%) nutrient levels compared to 2006). Increased leaflet toughness also may reduce low levels (1.2%). Higher fertility was obtained when herbivore feeding and therefore influence insect E. unguiculus was reared on plants in the high performance (Feeny 1970; Raupp 1985; Wheeler nutrient treatments. Therefore, an increase of leaflet and Center 1996). In this study, Brazilian peppertree nutrient content (N, P, K) improved insect perfor- plants exposed to high salinity conditions had tougher mance overall. These results are in agreement with mature leaflets and lower moisture content, which the Vigor Hypothesis (Price 1991), because negatively affected E. unguiculus survival. In con- E. unguiculus performed better on vigorous plants trast, Brazilian peppertrees irrigated only with growing under high nutrient levels. The Vigor freshwater had a higher specific leaflet area (SLA), Hypothesis proposes that plants growing under high which translates into thinner leaflets and lower resource availability allocate more resources to toughness. Similarly, high salinity levels have been replace plant tissue and less to secondary compounds shown to adversely affect the performance of cole- (Price 1991). Thus, E. unguiculus may prefer to feed opteran stem-borers (Hemminga and van Soelen on Brazilian peppertree plants growing in high 1988), and were detrimental to leaf-mining insects fertility soils in Florida, which may translate into (Schile and Mopper 2006). In addition, increased higher control of this invasive tree at those sites. salinity and decreased N availability negatively Brazilian peppertrees exposed to fresh-water envi- affected the gall density of Asphondylia borrichiae ronments were more nutritional host plants, as Rossi and Strong (Diptera: Cecidomyiidae) (Moon evidenced by the higher survivorship of E. ungui- and Stiling 2002). culus. Differences in plant parameters (e.g., leaflet Brazilian peppertree also is found in high-fertility nutrient contents, toughness, etc.) may explain the soils such as disturbed sites or former farmlands in changes in insect survival observed among salinity south and central Florida (Li and Norland 2001; Cuda treatments. For example, N and P leaflet content were et al. 2006). For example, the invasion of the higher in fresh-water environments compared to Everglades National Park by Brazilian peppertree saline environments, whereas K and Na were higher was facilitated by nutrient enrichment in abandoned in low and high-saline environments. Several studies farm soils in the Hole-in-the-Donut area (Li and have shown that nitrogen is a key factor limiting the Norland 2001). Results from this study showed that performance of insect herbivores, and an increase of Brazilian peppertree nutrient levels influenced the N availability usually improves larval survival, development and survival of E. unguiculus in the growth rate and reproduction of many insect species laboratory. Higher survival (40%) and fertility (89% 123 482 V. Manrique et al. eggs hatched) occurred in the high nutrient treat- Acknowledgments The authors are thankful to the ments, which contained higher leaflet nutrient content colleagues from the weed biological control laboratory (University of Florida) for their constant support and (N, P, K), lower toughness and higher moisture assistance during this study: J. Gillmore, J. C. Medal, content of leaflets. There is often a positive relation- R. Diaz, J. Markle, L. Markle, Y. Valenzuela, D. Gonzalez ship between nitrogen and insect performance and A. Samayoa. Special thanks to the collaborators in Brazil (Slansky and Feeny 1977; Mattson 1980; Wheeler for providing the insects: H. J. Pedrosa-Macedo (Federal University of Parana, Curitiba, Brazil), and M. Vitorino and Center 1996; Stiling and Moon 2005). In addition, (University of Blumenau, Brazil). This project was supported dietary water has a nutritional value for most insect by grants from the Florida Department of Environmental herbivores (Scriber 1979; Waring and Cobb 1992; Protection, South Florida Water Management District, Florida Huberty and Denno 2004), and increase in leaf water Exotic Pest Plant Council, and the Smithsonian Marine Station at Ft. Pierce. content has a positive effect on the growth perfor- mance of many lepidopteran species (Scriber 1979; Huberty and Denno 2004; Schoonhoven et al. 2005). References Moreover, tougher foliage due to water stress can reduce nitrogen availability and adversely affect Barkley FA (1944) Schinus L. Brittonia 5:160–198 performance of chewing insects (Huberty and Denno Barkley FA (1957) A study of Schinus L. Lilloa Revista de 2004). Another important factor to consider is plant Botanica. Tomo 28. 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