(Hydrilla Verticillata) Stem Quality

BIOLOGICAL CONTROL 8, 52–57 (1997) ARTICLE NO. BC960484

Growth and Development of the Biological Control Agent Bagous hydrillae as Inﬂuenced by Hydrilla (Hydrilla verticillata) Stem Quality

G. S. WHEELER AND T. D. CENTER USDA/ARS Aquatic Weed Research Unit, 3205 College Avenue, Ft. Lauderdale, Florida 33314

Received March 11, 1996; accepted August 28, 1996

that reduces the impact of insects imported for weed Plant quality of dioecious hydrilla was studied as a biological control. factor that may influence larval survival, growth, and The Australian weevil Bagous hydrillae O’Brien (Bal- development of the biological control agent Bagous ciunas and Purcell, 1991) was introduced into the hydrillae. Nitrogen content and stem toughness of United States for biological control of hydrilla. Release hydrilla varied among the five sites studied and be- of this species began in 1991, and to date, at least two tween summer and fall collections. The nitrogen con- field populations have established, one in Florida and tent of hydrilla collected during summer ranged from another in Texas (Center et al., unpublished data). 1.2 to 3.6% (dry weight) and during fall from 1.6 to 2.9%. Considerable difficulty has been experienced in estab- Stem toughness ranged from 487 to 940 g/mm2 during lishing this species despite release of several thousand the summer and from 418 to 1442 g/mm2 during the fall. individuals throughout the area. Among the factors The larvae of this weevil species required more time to that could influence weevil performance and establish- complete development when fed hydrilla containing ment, the quality of hydrilla, which varies greatly at lower levels of nitrogen and tougher stemmed plants. different sites (Zimba et al., 1993), may be of critical Moreover, pupal and adult fresh weights were also importance. The goal of this study was to determine the reduced when the larvae were fed the poorer quality effects of plant nitrogen and stem toughness on B. plants. Relative growth rates were reduced in larvae hydrillae larval survival, growth, and developmental fed hydrilla of lower nitrogen level and tougher plants. rates. Hydrilla plant quality constitutes an important factor that may limit the establishment and impact of this potential biological control agent. r 1997 Academic Press MATERIALS AND METHODS KEY WORDS: biological control of weeds; dioecious hydrilla; Curculionidae; Bagous hydrillae; leaf tough- Sites. Dioecious hydrilla samples were collected at ness; nitrogen. five sites in southeastern Florida that comprised a range of plant nitrogen content and plant toughness (Wheeler and Center, 1996). These sites included Lake Helen Blazes (HNB), located in Brevard County, and INTRODUCTION Sky Lake (SL), Miami Canal (MC), Hacienda Village (HV), and L-Lake (LL), all located in Broward County. It is widely recognized that plant quality influences These water bodies were flowing rivers or canals (HNB herbivore survival, growth, and development (Rosen- and MC) and artificial lakes (SL, HV, and LL), all of thal and Berenbaum, 1991, 1992; Stamp and Casey, which have been heavily infested with hydrilla consis- 1993). In addition to plant defenses, plant nutrient tently each year. Four hydrilla samples (about 500 g), content (Slansky, 1993; White, 1993) and physical separated by about 100 m, were collected from each characteristics (Grubb, 1986) may also influence herbi- site, consisting of a contiguous section of the upper 20 vore performance. For example, larvae of the ephydrid cm of the bed. From each sample, five apical shoot fly Hydrellia pakistanae Deonier fed relatively poor cuttings ca 20 cm in length, were measured for stem quality (low nitrogen levels and high leaf toughness) toughness; the remainder of the sample was used for plants of the aquatic weed hydrilla Hydrilla verticillata nitrogen determinations. The hydrilla at each site was (L.f.) Royle had increased mortality, decreased growth sampled during the summer (July) and fall (November– rates, and reduced adult weight compared with insects December). fed higher quality plants (Wheeler and Center, 1996). Plant quality. Hydrilla samples were analyzed for We predict that low plant quality is a common factor stem toughness with a gram gauge (Halda, Stockholm,

1049-9644/97 $25.00 52 Copyright r 1997 by Academic Press All rights of reproduction in any form reserved. B. hydrillae PERFORMANCE IS AFFECTED BY HYDRILLA PLANT QUALITY 53

Sweden) modified with a 0.53-mm-diameter blunt probe, (F 5 46.9; df 5 1,6; P 5 0.0005) during summer and which measured the pressure required to completely greater at HV (F 5 8.1; df 5 1,4; P 5 0.05) and LL penetrate each stem (Sands and Brancatini, 1991; (F 5 14.4; df 5 1,6; P 5 0.009; Fig. 1) during fall. Wheeler and Center, 1996). Stems were analyzed while Among-site analyses indicated that hydrilla from HNB on a Plexiglas stage equipped with a lid that held the had the greatest percentage of nitrogen during both stems in place. Holes in the lid and base acted as guides seasons. The hydrilla from HV and LL had the lowest for the insertion of the probe. Hydrilla stem toughness percentage of nitrogen during the summer, as did the was analyzed sequentially, starting with the point 5 cm hydrilla from MC and LL during fall (Fig. 1). from the apex of the shoot and cutting toward the base Stem toughness differed significantly by season at 5-cm intervals (i.e., 5, 10, 15, and 20 cm). Each (F 5 27.7; df 5 1,39; P , 0.0001), site (F 5 258.7; sample was submersed in a water-filled shoe box for 0 df 5 4,39; P , 0.0001), and distance from the tip to 3 days until ready for use. Percentage nitrogen of the (F 5 39.7; df 5 3,39; P , 0.0001; Fig. 2). Linear regres- hydrilla dry weight was determined with a modified sion indicated that stem toughness increased from the Kjeldahl method (Allen et al., 1974). tip toward the base during both seasons at all sites Weevil mortality, growth, and development. Bagous except HNB during summer and at SL during both hydrillae weevils were collected from our laboratory summer and fall (Fig. 2). colony (approximately 3 years in culture without infu- Weevil mortality, growth, and development. Percent- sion of wild individuals). Eggs were inserted individu- age mortality (mean 6 SE) of weevil larvae (summer, ally by hand into hydrilla stems within 5 cm of the tip. 26.0 6 4.8%; fall, 28.5 6 3.6%) was not influenced sig- Larvae (15 per site) were reared to pupation in petri nificantly by season or site. Larval development time dishes (15 3 3 cm) lined with moist filter paper and differed significantly by season (F 5 38.3; df 5 1,136; sealed with parafilm. The larvae were checked daily, P , 0.0001) and site (F 5 20.5; df 5 4,136; P , 0.0001). mortality was recorded, and fresh hydrilla stems were Moreover, the interaction of these two effects was added as needed. The length of time for the larvae to significant (F 5 7.8; df 5 4,136; P , 0.0001). Within- reach the prepupal, pupal, and adult stage was re- site comparisons indicated that larval development corded, as were pupal and adult weights using an times were significantly longer when fed hydrilla col- analytical balance (610 µg). Relative growth rates lected during the summer at all sites except HNB (Fig. (5RGR) of larvae were calculated according to the 3). Among-site comparisons indicated that during the following formula: fresh weight gained (mg)/average summer the larvae required the longest development fresh weight of the larva during the experiment (mg) · time when fed hydrilla from LL and the shortest time development time (Kogan, 1986). Adult gender was when fed hydrilla from HNB. Larvae fed the fall- determined by dissection and examination of the geni- collected hydrilla had the longest development times talia. when fed material from HV and MC, whereas the Data analysis. All analyses were conducted with shortest development times occurred on HNB hydrilla. SAS/PC, PROC GLM unless otherwise noted (SAS Pupal fresh weight differed significantly by season Institute, Inc., 1988). Nitrogen content and stem tough- (F 5 6.9; df 5 1,123; P 5 0.01) and site (F 5 7.3; ness were analyzed with a two-way analysis of variance df 5 4,123; P , 0.0001). Moreover, the interaction of (ANOVA), where site and season were the main effects. The influence of plant quality on larval developmental rates and adult weight was analyzed as a three-way factorial design, where site, season, and weevil sex were the main effects. Means were compared by the Ryan Q test (P 5 0.05). Linear regression (PROC REG; SAS Institute, 1988) was used to assess the relationship between RGR and leaf quality.

RESULTS

Plant quality. Tissue nitrogen concentrations varied among the five sites (F 5 130.1; df 5 4,27; P , 0.0001). As the interaction of the two effects FIG. 1. Mean (6SE) percentage of nitrogen of hydrilla collected (site 3 season) was significant (F 5 14.9; df 5 4,27; during two seasons from five sites in south Florida 1994. Within-site P , 0.0001), each effect was analyzed at fixed levels of differences in percentage of nitrogen between summer- and fall- collected hydrilla are indicated with an asterisk. Among-site compari- the other (Montgomery, 1984). Analysis of the effect of sons were not significantly different if the same uppercase letter season within each site indicated that nitrogen content appears above open bars (summer) or if the same lowercase letter was significantly greater in hydrilla from HNB appears above solid bars (fall). 54 WHEELER AND CENTER these two effects was significant (F 5 5.8; df 5 4,123; P 5 0.0003). Within-site comparisons indicated that pupal fresh weight differed between weevils fed summer- and fall-collected hydrilla only at HNB (F 5 27.5; df 5 1,37; P , 0.0001; Fig. 3). Among-site comparisons indicated that the larvae fed summer-collected hydrilla from HNB had the greatest pupal fresh weight, whereas the smallest pupae were produced from larvae fed LL hydrilla (Fig. 3). Larvae fed fall-collected hydrilla from SL had the greatest pupal fresh weight, whereas those fed the HV hydrilla had the lowest pupal fresh weight. Moreover, mean (6SE) pupal fresh weight was significantly greater for females (2.87 6 0.06 mg) than for males (2.51 6 0.05 mg; F 5 23.7; df 5 1,123; P , 0.0001). Adult fresh weight differed significantly by season (F 5 11.0; df 5 1,148; P 5 0.001) and site (F 5 5.2; df 5 4,148; P 5 0.0006). Moreover, the interaction of these two effects was significant (F 5 3.8; df 5 4,148; P 5 0.006). Within-site comparisons indicated that adult fresh weight differed between weevils fed summer- and fall-collected hydrilla only at HNB (F 5 16.6; df 5 1,31; P 5 0.0003) and the SL site (F 5 10.3; df 5 1,38; P 5 0.003; Fig. 3). Among-site comparisons indicated that the greatest adult fresh weight occurred when larvae were fed summer-collected hydrilla from HNB and the smallest adults were from larvae fed LL hydrilla (Fig. 3). The fresh weight of adults fed fall- collected hydrilla did not differ significantly. Moreover,

FIG. 3. Mean (6SE) performance of B. hydrillae larvae fed hydrilla collected during summer and fall at five sites in south Florida (1994). Within-site differences between summer- and fall- collected hydrilla are indicated with an asterisk. Among-site comparisons were not significantly different if the same uppercase letter appears above open bars (summer) or if the same lowercase letter appears above solid bars (fall). Adult fresh weight did not differ significantly for larvae fed hydrilla collected during fall.

the mean adult fresh weight was significantly greater for females (1.88 6 0.04 mg) than for males (1.56 6 0.03 mg; F 5 36.0; df 5 1,166; P , 0.0001). Linear regression analysis indicated that both percentage of nitrogen and leaf toughness significantly influenced larval RGR. Larval RGR decreased significantly when fed hydrilla consisting of low nitrogen content and greater stem toughness (Fig. 4). However, the same relationship was not found for larvae fed the fall-collected hydrilla.

DISCUSSION FIG. 2. Mean (6SE) stem toughness of hydrilla collected during summer and fall at five sites at different distances from the stem tip. Weevil larvae fed relatively high-quality hydrilla, All linear regressions were significant except HNB during summer containing high nitrogen levels and having soft stems, and SL during both seasons. Summer: HV r2 5 0.33, P , 0.0001; LL r2 5 0.18, P , 0.0001; MC r2 5 0.23, P , 0.0001. Fall: HNB r2 5 had increased performance compared with larvae fed 0.20, P , 0.0001; HV r2 5 0.25, P , 0.0001; LL r2 5 0.20, P , 0.0001; low-quality hydrilla. Although mortality was not signifi- MC r2 5 0.20, P , 0.0001. cantly affected, larval development time was shorter B. hydrillae PERFORMANCE IS AFFECTED BY HYDRILLA PLANT QUALITY 55

1993). Although fecundity was not assessed in our experiment, based upon the results of these studies relating increased fecundity to consumption of high- quality plants, we would expect a similar increase in the biotic potential of B. hydrillae fed the high-quality hydrilla. Nitrogen composition has been frequently shown to influence weevil performance; however, the results reported here, to our knowledge, are the first to demonstrate the importance of tissue toughness on weevil performance. As the hydrilla samples were field-collected, we could not control the interaction between the two plant factors monitored, percentage of nitrogen, and stem toughness. However, our results suggest, as do those of others (Loveless, 1962; Feeny, 1970; Hough and Pimen- tel, 1978; Van Soest, 1982; Coley, 1983; Potter and Kimmerer, 1986), that these factors are negatively correlated, as the nitrogen concentration was generally highest in plants with the lowest stem toughness (r 5 0.93; P 5 0.008 for the summer collections only). Percentage of nitrogen also decreased (Spencer et al., 1994; Wheeler and Center, 1996) and stem toughness increased from the growing tip toward the stem base. Data for terrestrial (reviewed by Wheeler and Center, 1996) and at least one floating aquatic plant species (Wright and Bourne, 1986) indicated that plant quality FIG. 4. Linear regression analysis of relative growth rates (RGR; decreased as plants age. Plant phenological stage can mg/mg · day) of B. hydrillae larvae as a function of percentage of also influence hydrilla quality, where percentage of nitrogen and stem toughness of hydrilla. Regression equations represent analysis of the means. Vertical lines represent standard nitrogen of hydrilla shoots decreased, as the plants errors of the means. changed from vegetative to reproductive nutrient allocation (Spencer et al., 1994). We expected that hydrilla quality would decrease as the plants changed their and pupal and adult weights were increased when the nutrient allocation to reproduction, induced by the larvae were fed higher quality hydrilla. For summer- decreasing day length of the fall season (Van et al., collected hydrilla, larval RGR increased significantly 1978). However, the quality of hydrilla in our experi- with increasing nitrogen levels and decreasing stem ment did not change consistently from summer to fall toughness. These results are similar to those of another (results supported by Boyd and Blackburn, 1970). The biological control agent of hydrilla, the ephydrid fly, H. percentage of nitrogen increased at two sites, decreased pakistanae, which also had increased performance when at one, and remained unchanged at two others. We did fed hydrilla with relatively high nitrogen content and not assess plant age in our experiments. Possibly, soft leaves (Wheeler and Center, 1996). Increases in collections of hydrilla from the same plants, instead of performance also occurred in other weevil species fed randomly selected plants, during different seasons high quality food. Increased egg production and de- would have produced results of decreasing quality as creased preoviposition periods occurred in the black the plant aged. If this seasonal decrease in hydrilla vine weevil (Brachyrhinus sulcatus (F.)) when fed straw- quality does occur, as we suggest, it may significantly berry plants containing relatively high levels of nitro- decrease the growth and development of the weevil gen (Cram, 1965a,b). Fecundity increased in boll wee- larvae. vils when the adults were fed artificial diets containing Herbivore growth and development can be influenced higher nitrogen levels (Hilliard and Keeley, 1984a,b) by plant-quality factors, two of which consistently and in Cyrtobagous salviniae Calder and Sands when include nitrogen and toughness. The nitrogen values the weevils were fed salvinia fertilized with nitrogen expressed in this study represent the levels present in (Sands et al., 1983; Room et al., 1989). Moreover, both the leaves and stems combined. However, herbi- increased performance (increased survival, decreased vore feeding is frequently much more selective, and in development time, and increased adult weight) oc- the case of B. hydrillae, weevil larvae feed inside the curred with Hylobius weevils fed nitrogen-treated pines stems. Nitrogen levels in hydrilla plants are higher in compared with lower nitrogen treatments (Hunt et al., leaves (1.5- to 1.7-fold) than in stems (Guha, 1965) and 56 WHEELER AND CENTER therefore the dietary nitrogen levels are probably much control of weeds has been demonstrated in several lower than that reported here. Moreover, we measured notable examples (Dodd, 1940; Room et al., 1981; the pressure needed to penetrate the entire hydrilla Taylor, 1984; Wheeler and Center, 1996). Nitrogen stem with our penetrometer device. However, the fe- content of the host plant has played a key role in the male weevils penetrate the outer stem epidermis before establishment of a few biological control agents and in ovipositing in the stems (Balciunas and Purcell, 1991). the production of outbreak populations of exotic and This behavior undoubtedly benefits the first instars as native herbivorous insects (Myers, 1987). The results they begin to feed and bore through the stem tissues. reported here indicate that hydrilla grown at different Although our measurements of these plant-quality sites differed in nutritional quality and that these factors may not have assessed the quality of the actual differences influenced the relative growth rates of the tissues consumed, they do approximate those values. weevil larvae. Although larval mortality was not af- Further studies that evaluate the quality of the tissues fected, the impact of these nutritional differences on actually consumed on insect performance and the effect larval performance may limit the establishment of this of each plant-quality factor separately with minimal species to sites with nitrogen-rich, soft-textured hy- variation in other factors are needed. drilla. High toughness of the plant tissue may be related to high concentrations of tissue lignin and fiber (Buend- ACKNOWLEDGMENTS gen et al., 1990; Choong et al., 1992), constituents that decrease the digestibility of the ingested food (Martin, We thank R. Leidi-Ferrer, A. Bishop, W. Durden, and A. Durden for 1987; Wheeler and Slansky, 1991) and potentially technical assistance and D. F. Spencer (USDA/ARS, Davis CA), G. R. Buckingham (USDA/ARS, Gainesville, FL), and A. D. Wright (CSIRO, restrict the movement of and consumption by small Indooroopilly,Australia) for valuable comments on a previous draft of internal feeding leaf miners and stem borers (Hagen the manuscript. Financial support was provided by the Southwest and Chabot, 1986; Kimmerer and Potter, 1987). Further- Florida Water Management District, Florida Department of Environ- more, the penetration of plant tissues by these internal mental Protection, and the U.S. Army Corps of Engineers. feeders may be impeded, as suggested by preliminary studies with H. pakistanae (Wheeler, unpublished re- REFERENCES sults), where the first instars apparently experienced considerable difficulty penetrating the tougher leaves Allen, S. E., Grimshaw, H. M., Parkinson, J. A., and Quarmby, C. of hydrilla, resulting in nearly 100% mortality. The 1974. ‘‘Chemical Analysis of Ecological Materials.’’ Blackwell Scien- negative impact of low plant nutrient levels can be tific, Oxford, UK. Balciunas, J. K., and Purcell, M. F. 1991. Distribution and biology of a augmented by natural enemies, as exposure time to new Bagous weevil (Coleoptera: Curculionidae) which feeds on the these biotic mortality factors may be increased (Dam- aquatic weed, Hydrilla verticillata. J. Aust. Entomol. Soc. 30, man, 1987; Stamp and Bowers, 1990). 333–338. Water velocity can influence the species composition Boyd, C. E., and Blackburn, R. D. 1970. Seasonal changes in the and the quality of the plants in a water body (Haslam, proximate composition of some common aquatic weeds. Hyacinth 1978). For example, several submersed aquatic species Contr. J. 8, 42–44. (curleyleaf pondweed, elodea, and Eurasian watermil- Buendgen, M. R., Coors, J. G., Grombacher, A. W., and Russell, W. A. 1990. European corn borer resistance and cell wall composition of foil) grown in flowing water (0.25 to 0.67 m/s) had three maize populations. Crop Sci. 30, 505– 510. greater fiber content (acid detergent fiber), but no Choong, M. F., Lucas, P. W., Ong, J. S. Y., Pereira, B., Tan, H. T. W., significant difference in nitrogen content, compared and Turner, I. M. 1992. Leaf fracture toughness and sclerophylly: with plants from static water bodies (Pine et al., 1991). their correlations and ecological implications. New Phytologist 121, The herbivorous grass carp (Ctenopharyngodon idella 597–610. Val.) ate significantly more of the low fiber, static Coley, P. D. 1983. Herbivory and defensive characteristics of tree species in a lowland tropical forest. Ecol. Monogr. 53, 209–233. water-body plants compared with the high-fiber indi- Cram, W. T. 1965a. Fecundity of the root weevils Brachyrhinus viduals. Our results from hydrilla collected in canals sulcatus and Sciopithes obscurus on strawberry at different condi- (HNV and MC), where water flow is barely detectable, tions of host plant nutrition. Can. J. Plant Sci. 45, 219–225. did not support these reports; in fact, the hydrilla from Cram, W. T. 1965b. Fecundity of the black vine weevil on strawberry these sites was among the softest sampled. Possibly, with nitrogen supplied in the ammonium or nitrate form. Can. J. hydrilla will develop tougher tissues when grown in Plant Sci. 45, 295–296. greater flow velocities, such as near spring boils, which Damman, H. 1987. Leaf quality and enemy avoidance by the larvae of in Florida may reach 0.2 m/s (Odum, 1957). If hydrilla a pyralid moth. Ecology 68, 88–97. Dodd, A. P. 1940. ‘‘The Biological Campaign against Prickly Pear.’’ toughness and fiber content increases in high velocity Commonwealth Prickly Pear Board, Brisbane, Australia. water bodies, we expect that it will be more resistant to Feeny, P. P. 1970. Seasonal changes in oak leaf tannins and nutrients attack by our two biological control agents H. paki- as a cause of spring feeding by winter moth caterpillars. Ecology stanae and B. hydrillae. 51, 565–581. The importance of plant quality in the biological Grubb, P. J. 1986. Sclerophylls, pachyphylls and pycnophylls: the B. hydrillae PERFORMANCE IS AFFECTED BY HYDRILLA PLANT QUALITY 57

nature and significance of hard leaf surfaces. In ‘‘Insects and the suffer most from herbivores: Latitude, nitrogen and biological Plant Surface’’ (B. E. Juniper and T. R. E. Southwood, Eds.), pp. control of the weed Salvinia molesta. Oikos 54, 92–100. 137–150. Edward Arnold, London. Rosenthal, G. A., and Berenbaum, M. R. 1991. ‘‘Herbivores: Their Guha, J. 1965. Diurnal variation of the carbohydrate and nitrogen Interactions with Secondary Plant Metabolites: The Chemical contents in the leaves and stems of Hydrilla verticillata Casp. Participants,’’ 2nd ed., Vol. 1. Academic Press, New York. during its vegetative phase. Bot. Soc. Bengal 18, 28–31. Rosenthal, G. A., and Berenbaum, M. R. 1992. ‘‘Herbivores: Their Hagen, R. H., and Chabot, J. F. 1986. Leaf anatomy of maples (Acer) Interactions with Secondary Plant Metabolites: Ecological and and host use by Lepidoptera larvae. Oikos 47, 335– 345. Evolutionary Processes,’’ 2nd ed., Vol. 2. Academic Press, New York. Haslam, S. M. 1978. ‘‘River Plants: The Macrophytic Vegetation of Sands, D. P. A., and Brancatini, V. A. 1991. A portable penetrometer Watercourses.’’ Cambridge Univ. Press, Cambridge, UK. for measuring leaf toughness in insect herbivory studies. Proc. Hilliard, R. A., and Keeley, L. L. 1984a. Interactions between dietary Entomol. Soc. Washington 93, 786– 788. nitrogen and simulated autumn conditions on diet consumption Sands, D. P. A., Schotz, M., and Bourne, A. S. 1983. The feeding and reproductive development in the boll weevil, Anthonomus characteristics and development of larvae of a Salvinia weevil grandis. Physiol. Entomol. 9, 417–423. Cyrtobagous sp. Entomol. Exp. Appl. 34, 291–296. Hilliard, R. A., and Keeley, L. L. 1984b. The effects of dietary nitrogen SAS Institute 1988. SAS/STAT User’s Guide Release 6.08. SAS on reproductive development in the female boll weevil, Anthono- Institute, Cary, NC. mus grandis. Physiol. Entomol. 9, 165–174. Slansky, F. J. 1993. Nutritional ecology: The fundamental quest for Hough, J. A., and Pimentel, D. 1978. Influence of host foliage on nutrients. In ‘‘Caterpillars: Ecological and Evolutionary Con- development, survival, and fecundity of the gypsy moth. Environ. straints on Foraging’’ (N. E. Stamp and T. M. Casey, Eds.), pp. Entomol. 7, 97–102. 29–91. Chapman and Hall, New York. Hunt, D. W. A., Lintereur, G., Salom, S. M., and Raffa, K. F. 1993. Spencer, D., Anderson, L., Ksander, G., Klaine, S., and Bailey, F. 1994. Performance and preference of Hylobius radicis Buchanan, and H. Vegetative propagule production and allocation of carbon and pales (Herbst) (Coleoptera: Curculionidae) on various Pinus spe- nitrogen by monoecious Hydrilla verticillata (L.f.) Royle grown at cies. Can. Entomol. 125, 1003–1010. two photoperiods. Aquat. Bot. 48, 121–132. Kimmerer, T. W., and Potter, D. A. 1987. Nutritional quality of specific Stamp, N. E., and Bowers, M. D. 1990. Variation in food quality and leaf tissues and selective feeding by a specialist leafminer. Oecolo- temperature constrain foraging of gregarious caterpillars. Ecology gia 71, 548–551. 71, 1031–1039. Kogan, M. 1986. Bioassays for measuring quality of insect food. In Stamp, N. E., and Casey, T. M. 1993. ‘‘Caterpillars: Ecological and ‘‘Insect–Plant Interactions’’ (J. R. Miller and T. A. Miller, Eds.), pp. Evolutionary Constraints on Foraging.’’ Chapman & Hall, New 155–189. Springer-Verlag, New York. York. Loveless, A. R. 1962. Further evidence to support a nutritional Taylor, M. F. J. 1984. The dependence of development and fecundity interpretation of sclerophylly. Ann. Bot. 26, 551–561. of Samea multiplicalis on early larval nitrogen intake. J. Insect Martin, M. M. 1987. ‘‘Invertebrate–Microbial Interactions. Ingested Physiol. 30, 779–785. Fungal Enzymes in Arthropod Biology.’’ Comstock Publishing, Van Soest, P. J. 1982. ‘‘Nutritional Ecology of the Ruminant.’’ O & B Ithaca, NY. Books, Corvallis, OR. Montgomery, D. C. 1984. ‘‘Design and Analysis of Experiments,’’ 2nd Van, T. K., Haller, W. T., and Garrard, L. A. 1978. The effect of ed. Wiley, New York. daylength and temperature on hydrilla growth and tuber produc- Myers, J. H. 1987. Population outbreaks of introduced insects: tion. J. Aquat. Plant Manage. 16, 57–59. Lessons from the biological control of weeds. In ‘‘Insect Outbreaks’’ Wheeler, G. S., and Center, T. D. 1996. The influence of hydrilla leaf (P. Barbosa and J. C. Schultz, Eds.), pp. 173–193. Academic Press, quality on larval growth and development of the biological control New York. agent Hydrellia pakistanae (Diptera: Ephydridae). Biol. Control 7, Odum, H. T. 1957. Trophic structure and productivity of Silver 1–9. Springs, Florida. Ecol. Monogr. 27, 55–112. Wheeler, G. S., and Slansky, F. J. 1991. Compensatory responses of Pine, R. T., Anderson, L. W. J., and Hung, S. S. O. 1991. Plant the fall armyworm (Spodoptera frugiperda.) when fed water- and preferences of triploid grass carp. J. Aquat. Plant Manage. 29, cellulose-diluted diets. Physiol. Entomol. 16, 361–374. 80–82. White, T. C. R. 1993. ‘‘The Inadequate Environment: Nitrogen and Potter, D. A., and Kimmerer, T. W. 1986. Seasonal allocation of the Abundance of Animals.’’ Springer-Verlag, New York. defense investment in Ilex opaca Aiton and constraints on a Wright, A. D., and Bourne, A. S. 1986. Effect of leaf hardness on specialist leafminer. Oecologia 69, 217–224. penetration of waterhyacinth by Sameodes albiguttalis. J. Aquat. Room, P. M., Harley, K. L. S., Forno, I. W., and Sands, D. P. A. 1981. Plant Manage. 24, 91–92. Successful biological control of the floating weed Salvinia molesta. Zimba, P. V., Hopson, M. S., and Colle, D. E. 1993. Elemental Nature 294, 78– 80. composition of five submersed aquatic plants collected from Lake Room, P. M., Julien, M. H., and Forno, I. W. 1989. Vigorous plants Okeechobee, Florida. J. Aquat. Plant Manage. 31, 137–140.