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1 June 2013 Temperature-Dependent Reproductive and Life Table Parameters of Elasmopalpus lignosellus (Lepidoptera: Pyralidae) on Sugarcane
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Abstract

The lesser cornstalk borer, Elasmopalpus lignosellus (Zeller) (Lepidoptera: Pyralidae) is an important pest of sugarcane (a complex hybrid of Saccharum spp.) in southern Florida. Reproductive and life table parameters for E. lignosellus were examined at nine constant temperatures from 13 to 36 °C with sugarcane as the larval food source. The pre- and post-oviposition periods decreased with increasing temperatures and reached their minimums at 33 and 36 °C, respectively. The oviposition period was longest at 27 °C. The mean fecundity, intrinsic rate of increase (r), and finite rate of increase (λ) were greatest at 30 °C and decreased with increasing or decreasing temperature. The net reproductive rate (R0) was greatest at 27 °C. The Brière-1 model best described the relationship between temperature and r. The generation (T) and population doubling times (DT) were shortest at 33 and 30 °C, respectively. The temperatures around 27 to 30 °C are most favorable for E. lignosellus population growth and significant damage can be expected under these climatic conditions. This data in combination with population monitoring of E. lignosellus under field conditions can be effectively used in population predictions of this pest in field and severe damage can be prevented by timely implementation of control measures.

Sugarcane (a complex hybrid of Saccharum spp.) (Poales: Poaceae) is an important crop grown in many southern temperate through tropical regions of the world [United States Department of Agriculture (USDA 2012)]. Florida, Louisiana, Texas and Hawaii are the main sugarcane producing states in the USA. Florida was the leading sugarcane producing state in the U.S. in 2010 with 392,000 acres (158,600 ha) (397,000 acres [160,700 ha] in 2011). The total value of Florida sugarcane in 2010 was $492.9M (USDA 2012). The lesser cornstalk borer, Elasmopalpus lignosellus (Zeller) (Lepidoptera: Pyralidae), is a polyphagous, semi-subterranean pest that is widely distributed in USA and Central and South America (Heinrich 1956; Genung & Green 1965; Chang & Ota 1987). Eggs are deposited mostly on the soil surrounding plants. Larvae bore into sugarcane stems below the soil surface and produce a silken tunnel at the entrance hole outward into the soil from which they attack the plants, as well as rest, molt and pupate (Schaaf 1974). Elasmopalpus lignosellus requires 548 degree days to complete development on sugarcane with lower and upper developmental thresholds estimated at 9.3 and 37.9 °C, respectively (Sandhu et al. 2010). Dead heart symptoms are produced when larvae reach the center of the shoot and damage or sever the youngest leaves or apical meristem. Non-lethal damage is caused when larvae chew only a few mm into the shoot evidenced by several symmetrical rows of holes revealed as the leaves emerge from the whorl. Larval feeding damage reduces plant stand and vigor, sugarcane photosynthesis, number of millable stalks and sugar yield (Carbonell 1977).

Reproductive studies of the lesser cornstalk borer have been conducted on cowpeas or southern peas (Luginbill & Ainslei 1917; Dupree 1965), peanuts (King et al. 1961), soybean (Leuck 1967), and sugarcane (Carbonell 1978). In all these studies, temperature and relative humidity were allowed to vary with the climatic conditions. Stone (1968) and Mack & Backman (1984) reported the longevity and oviposition rates of E. lignosellus on an artificial diet under controlled environmental conditions. However, quantitative information on life table parameters, such as intrinsic rate of increase (r), net reproductive rate (R0), finite rate of increase (λ), mean generation time (T), and population doubling time (DT) was not published in their studies.

Life tables are powerful tools for analyzing and understanding the impact of external factors such as temperature on the growth, survival, reproduction, and rate of increase of insect populations (Sankeperumal et al. 1989). The intrinsic rate of increase can vary with the larval host or diet (Carey 2003). For example, female Helicoverpa assulta Guenee (Lepidoptera: Noctuidae) reared as larvae on artificial diet had significantly greater r values than females reared as larvae on pepper (Capsicum frutescens L.) (Solanales: Solanaceae) (Wang et al. 2008). To predict the lesser cornstalk borer population parameters on sugarcane, it is important to study its life history on the same host. Development and survivorship rates for E. lignosellus reared on sugarcane at constant temperatures were determined in a recent study (Sandhu et al. 2010). The purpose of this experiment was to measure the effect of a range of constant temperatures on reproductive (pre-oviposition, oviposition, post-oviposition periods, and fecundity) and life table parameters (r, R0, λ, T, and DT) of the lesser cornstalk borer reared on sugarcane.

MATERIALS AND METHODS

Reproductive Parameters

Pre-oviposition, oviposition, post-oviposition periods, and fecundity for E. lignosellus were determined at nine constant temperatures [13, 15, 18, 21, 24, 27, 30, 33, and 36 °C (± 0.05 °C)] at 14:10 (L:D) and 65–70% RH in temperature controlled chambers (Custom made, Department of Entomology and Nematology, University of Florida, Gainesville, FL) to construct time-specific life tables. This study was conducted in 2006–2008. Using two chambers, two temperatures were tested simultaneously with pairs of temperatures tested staggered over time. The range of tested temperatures was selected based on those experienced by lesser cornstalk borer in sugarcane in southern Florida. The experiment design was a randomized complete block with three cohorts at each temperature and it was replicated through time; repeated for three generations at each temperature. Adults were obtained from immatures reared on sugarcane used for companion developmental studies (Sandhu et al. 2010) conducted at the same temperatures and relative humidity as indicated above. Details on materials and methods used to rear immature stages are available in Sandhu et al. (2010). Ten male:female pairs of newly emerged adults (< 12 h old) were first released into each of three oviposition cages (17 × 17 × 17 cm) to facilitate mating. Adults were provided with a 10% honey solution for free feeding (ad libitum feeding), because sugarcane does not produce a food source for adults. After 24-h, individual pairs were moved to transparent plastic cylinders (one pair per cylinder) (11 cm length and 5 cm diameter; Thornton Plastic Co., Salt Lake City, UT) lined with tubular synthetic stockinette (Independent Medical Co-Op, Ormond Beach, FL) as an oviposition substrate as the females prefer rough, dry substrates for oviposition. We used stockinette because females preferred it over the Handy Wipes (The Chlorox Co., Oakland, CA) used by previous workers (e.g., Chalfant 1975). Adults were observed daily to record the limits of the reproductive parameters. The stockinette was replaced daily during oviposition periods. The orange-colored eggs were easily observed against the white background of the material and were counted using a hand lens. Fecundity was reported as the number of eggs deposited by an individual female during her entire life period. Age-specific female survival (lx, percentage of females alive at specific age x) and age-specific fecundity (mx, number of female offspring produced by a female in a unit of time) were recorded for each day (x) they were alive. Age specific fecundity was calculated as (f / (m + f)) × n, where f = number of females, m = number of males, and n = number of offspring. The lx and mx were calculated for each cohort of 10 females. Age-specific survivorship curves were constructed using adult lx and mx values for cohorts at each temperature treatment.

Life Table Parameters

The age-specific life table method was used to calculate the life table parameters for E. lignosellus (Birch 1948). The values of lx used in life table calculations were obtained by combining age specific adult female survival with the survival of immatures reported under same environmental conditions in a concurrent study (Sandhu et al. 2010). Similarly, the age of adults (x) used in these calculations also includes the development time of immatures reared on sugarcane under the same environmental conditions (Sandhu et al. 2010). The intrinsic rate of increase (r) was calculated through iteration of the Euler-Lotka equation (Σe-rx lxmx = 1). The lx and mx values were used to calculate the net reproductive rate (R0 = Σlxmx, mean number of female offspring / female) and the mean generation time (T = Σ(xlxmx) / Σ(lxmx), mean age of the mothers in a cohort at the birth of female offspring). The values for r at each temperature were used to calculate the finite rate of increase (λ = er, the number of times the population multiplies in a unit of time) and population doubling time (DT = ln (2) / r, the time required for the population to double). To compare the thermal sensitivities of r and R0, we plotted these alternative fitness measures against the tested temperatures.

TABLE 1.

MATHEMATICAL EQUATIONS OF THE MODELS TESTED TO DESCRIBE THE RELATIONSHIP BETWEEN TEMPERATURE AND INTRINSIC RATE OF INCREASE IN LESSER CORNSTALK BORER ON SUGARCANE.

Model Evaluation

A non-linear distribution was observed when r was plotted against the temperature treatments. To find an equation that best fit the observed relationship between r and temperature, eight non-linear models (Table 1) previously used (Roy et al. 2003; Bonato et al. 2007; Sandhu et al. 2010; Shi & Ge 2010) to describe temperature dependent development or other population parameters of different insects were tested. The parameters of the nonlinear models were estimated with the nonlinear regression model of Marquardt (1963) using SAS (SAS Institute 2008). Sigma Plot (Systat Software, Inc., San Jose, CA) was used to plot the regressions of the non-linear models. The models were evaluated based on the coefficient of determination (r2), the adjusted coefficient of determination (r2adj, a modified r2 that adjusts for the number of explanatory terms in the model), the residual sum of squares (RSS), and the corrected Akaike Information Criterion (AICC) (Burnham and Anderson 2004). The r2 and r2adj. indicate better fits with higher values, whereas RSS and AICC indicate better fits with lower values. The corrected AIC value was calculated using the formula:

e01_380.gif
where n denotes the sample size; RSS denotes the residual sum of squares; K is the number of model parameters including an error item (namely the number of free parameters in the model itself). The AICC was preferred over the AIC because of the small sample sizes (n/K < 40) in this study, for which AICC is recommended (Hurvich & Tsai 1989; Burnham & Anderson 2004).

Statistics

PROC MIXED (SAS Institute 2008) was used to analyze the variance due to the potential covariance structure associated with taking repeated measures over time at each temperature. Normality of the data was tested with the Shapiro-Wilk normality test (Shapiro & Wilk 1965). The oviposition cages were treated as cohorts and replications through time were treated as generations for data analysis. Temperatures, cohorts, generations, and their interactions were used in the analysis of variance models. Generations were used as the repeated variable and the cohorts were nested under temperature in the repeated measures statement. Several covariance structures were fitted to the data. The unstructured covariance type fit well and was used for the analysis (Littell et al. 1998). Data for each pair of adults were used for analysis of effects of temperature, cohort, and generation for reproductive parameters. Daily values by cohort were used for analysis of effects of temperature and generation on lx and mx. The percentage of females alive at age x (lx) was arcsin square root transformed for normality purposes before analysis and retransformed for presentation purposes. The Tukey's HSD test (SAS Institute 2008) was used for means separation with α = 0.05.

RESULTS

Reproduction

Temperature significantly affected the lengths of the lesser cornstalk borer pre-oviposition, oviposition, and post-oviposition periods (Table 2). Cohorts, generations and the modeled interactions were not significant sources of variation in the models for any of these periods. Therefore, data were pooled across cohorts and generations to calculate means for these periods. The mean pre-oviposition period decreased with an increase in temperature from 9.7 d at 13 °C to 2.3 d at 33 °C (Table 3). The mean oviposition period was longest (5.6 d) at 27 °C and decreased with an increase or decrease in temperature from 27 °C. The post-oviposition period became progressively shorter from a maximum at 13 °C to a minimum at 36 °C (Table 3).

TABLE 2.

ANALYSIS OF VARIANCE FOR EFFECTS OF TEMPERATURE, COHORT AND GENERATION ON REPRODUCTIVE PARAMETERS OF ELASMOPALPUS LIGNOSELLUS ON SUGARCANE.

TABLE 3.

MEAN (± SEM) PRE-OVIPOSITION, OVIPOSITION, POST-OVIPOSITION PERIODS AND FECUNDITY FOR ELASMOPALPUS LIGNOSELLUS ON SUGARCANE.

Fecundity was also significantly affected by temperature (Table 2). Cohort, generation and modeled interactions were not significant sources of variation in the fecundity model. Therefore, the fecundity data were pooled across cohorts and generations to calculate mean fecundity at each temperature. Fecundity increased with an increase in temperature from 13 to 30 °C and decreased at 33 and 36 °C. Mean fecundity ranged from 29.2 (13 °C) to 165.3 eggs (30 °C) (Table 3) which indicates that warm temperatures are more favorable for fecundity than cool temperatures.

LIFE TABLE PARAMETERS

Temperature had a significant effect on lx (F = 50.19; df = 8, 333; P < 0.0001) and mx values (F = 16.05; df = 8, 333; P < 0.0001). Generations and the modeled interactions did not provide significant sources of variation in the models for lx (F = 0.52; df = 2, 333; P = 0.5972; F = 0.75; df = 16, 333; P = 0.7384) or mx (F = 0.13; df = 2, 333; P = 0.8805; F = 0.26, df = 16, 333, P = 0.9984). Therefore, the data were pooled across generations to calculate means for these periods. Both lx and mx increased with an increase in temperature from 13 to 27 °C and then decreased at or above 33 °C except at 15 °C where mx was unexpectedly greater than 18, 21, and 24 °C (Fig. 1).

Data were pooled across generations (i.e., 90 different pairs were pooled for each temperature, total 810 pairs) to calculate the life table parameters r, R0, λ, T, and DT at each temperature, because pre-oviposition, oviposition, post-oviposition and fecundity were significantly affected by temperature, but not by cohort or generation (Table 2). The intrinsic rate of increase (r) and the finite rate of increase (λ) both increased with an increase in temperature from 13 to 30 °C before starting to decrease at > 33 °C (Table 4). The negative value of r at 13 °C (-0.0021) indicates a decrease rather than an increase in lesser cornstalk borer population with time at this temperature. The net reproductive rate (R0) was greatest at 27 °C (53.8537). Comparing the values of r and R0 versus temperature resulted in similar increases to maximum values, but the curve for r was shifted slightly to the right of the curve for R0 (Fig. 2). The mean generation time (T) decreased from the maximum at 13 °C (130.7 d) to the minimum at 33 °C (27.7 d) (Table 4). The population doubling time (DT) was negative (-334.8537) at 13 °C which indicates that the population will reduce to half of its original population in 334.9 days rather than increase in population. The value of DT was lowest (5.6386) at 30 °C which means population doubles in size in 5.6 days at this temperature.

Model Evaluation

The model evaluation parameters, and the predicted optimum temperatures (temperatures for maximum intrinsic rate of increase) are presented in Table 5. The predicted optimum temperature ranged from 28.8 °C (Taylor model) to 31.3 °C (Logan model). In general, all the tested models showed satisfactory fitted results with r2> 0.9312 and r2adj > 0.8623. The polynomial (fourth order) and Wang-Lan-Ding models showed the best fit to the data based on their higher r2and r2adj and lower RSS values than other models (Table 5). However, the greater number of fitted parameters in the polynomial model resulted in greater AICC value (-39.09) than the other models and the AICC for Wang-Lan-Ding could not be calculated, because (n-K-1) in the AICC formula equaled zero. Based on the lowest AICC (-62.43) values, the Brière-1 was found to be the best model to describe the relationship between r and temperature.

Fig. 1.

Relationships between the adult age (d) and age-specific survival lx (solid line) and age specific daily fecundity mx (dashed line) for Elasmopalpus lignosellus at 9 constant temperatures.

f01_380.jpg

The fitted curves for all the tested models representing the relationship between r and temperature for the lesser cornstalk borer on sugarcane are presented in Figs. 3a and 3b. In general, the shape of these curves estimated by different models is quite similar. However, some models had different lower and upper temperatures where the curve intersected x-axis. For example, in Brière-1, Brière-2, Lactin, Ratkowsky and Wang-Lan-Ding models, curve intersected the x-axis at approximately 12–13 °C which indicates their estimated lower temperature threshold. However, in Logan and Taylor models, curve did not intersect x-axis at lower temperature which indicate the estimated lower temperature threshold to be < 10 °C. Similarly, the estimated upper temperature threshold was 36–37 °C in most of the models, but in Taylor model it was > 40 °C, because curve did not intersect x-axis even at 40 °C.

TABLE 4.

LIFE TABLE PARAMETERS FOR ELASMOPALPUS LIGNOSELLUS ON SUGARCANE AT NINE CONSTANT TEMPERATURES.

Fig. 2.

Effect of temperature (°C) on Elasmopalpus lignosellus intrinsic rate of increase (r) and net reproductive rate (R0 ).

f02_380.jpg

DISCUSSION

Reproduction

The values for reproductive parameters on sugarcane fell mostly within the ranges of those determined for E. lignosellus on other crops such as southern pea and soybean. The mean (± SEM) pre-oviposition period found in this study (2.3 ± 0.05 d at 33 °C to 9.7 ± 0.06 d at 13 °C) is similar to the value of 2.8 d reported by Stone (1968) for E. lignosellus on an artificial diet at 27 °C. The mean oviposition period on sugarcane (2.2 ± 0.05 d at 13 °C to 5.6 ± 0.06 d at 27 °C) was shorter than those reported on artificial diets (10.4 d, Luginbill and Ainslei 1917; 11.8 d, Stone 1968; and 6.4 d, Simmons and Lynch 1990), but within the range determined by Dupree (1965) on southern pea (mean: 4.1 d, range 1 to 9 d). The 4.7 d post-oviposition period reported by Leuck (1967) on soybean is consistent with that found on sugarcane (2.5 ± 0.05 to 5.9 ± 0.07 d).

Fecundity on sugarcane (29 to 165 eggs per female) mostly fell within the range reported by others on leguminous crops and artificial diets. The lesser cornstalk borer mean fecundity (number of eggs/female) reported in earlier studies was 192 on cowpeas (Luginbill & Ainslei 1917), ranged from 124 to 129 on soybean (King et al. 1961; Dupree 1965; Leuck 1967), and ranged from 67 (Calvo 1966) to 419.5 on artificial diet (Stone 1968). The results of our study are similar to those of Mack and Backman (1984) who reported an increase in fecundity with an increase in temperature from 17 to 27.5 °C, peaks at 27.5 and 30.5 °C, and large decreases at 17 and 35 °C.

Life Table Parameters

Elasmopalpus lignosellus reached its maximum reproductive rate within the same temperature range where generation time and population doubling time were the lowest (30 to 33 °C). Life table parameters for lesser cornstalk borer on other hosts are not available for comparison, but such values have been published for other stalk boring Lepidoptera pests of monocots (Table 6). Intrinsic rate of increase (r) at 25 °C on corn and artificial diet for Diatraea lineolata (Walker) (Lepidoptera: Crambidae), a neotropical cornstalk borer (Rodríguez-del-Bosque et al. 1989), were slightly lower than those found in this study for E. lignosellus that developed as larvae on sugarcane at 24 °C. The sugarcane borer, D. saccharalis (F.), and the Mexican rice borer, Eoreuma loftini (Dyar) (both Lepidoptera: Crambidae), recorded lower r and λ, and higher T and DT parameters at 30 °C on an artificial diet that included dried, ground sugarcane leaf sheaths (Sétamou et al. 2002) than those reported in our study for E. lignosellus. The Mexican rice borer had greater R0 than the lesser cornstalk borer that indicates its high reproductive potential, but the r for the Mexican rice borer was lower on an artificial diet than for the lesser cornstalk borer on sugarcane. Our studies determined that r and λ for E. lignosellus reared on sugarcane were slightly lower than D. saccharalis reared on corn and on sugarcane at 27 °C (Bessin & Reagan 1990). However, the net reproductive rate (R0) for D. saccharalis on both of these host plants was approximately seven times greater than for E. lignosellus on sugarcane. The results of Bessin & Reagan (1990) and Sétamou et al. (2002), who found very different r and R0 values for D. saccharalis that developed on corn and sugarcane compared to an artificial diet containing <10% sugarcane leaf sheaths, provide further evidence that larval host or diet affects the intrinsic rate of increase.

TABLE 5.

COMPARISON OF DIFFERENT NON-LINEAR MODELS TESTED TO DESCRIBE THE RELATIONSHIP BETWEEN INTRINSIC RATE OF INCREASE (r) AND TEMPERATURE (°C).

Fig. 3a–b.

Relationship between temperature (°C) and intrinsic rate of natural increase (r) for E. lignosellus on sugarcane described by different non-linear models.

f03_380.jpg

TABLE 6.

LIFE TABLE PARAMETERS FOR SELECTED STEM-BORING LEPIDOPTERA PESTS OF SUGARCANE AND CORN.

In most ectotherms, r reaches its maximum value at a greater temperature than for R0. Huey & Berrigan (2001) attributed this to r (but not R0) being sensitive to the accelerating effect of high temperature on generation time. Because r is inversely related to generation time and R0 is independent of it (Cole 1954; Lewontin 1965), the normal shortening of the generation time associated with rising temperatures will work to increase r without affecting R0. This leads to a shift to the right in the thermal fitness curve for r relative to R0, as was observed in this study. This right shift of the r curve relative to the R0 curve observed for E. lignosellus on sugarcane may be due to the shortest generation time occurring at a temperature 3 and 6 °C greater than the maximum r and R0 values, respectively.

Model Evaluation

Mathematical models used in this study were also tested to describe the relationship between temperature and r for Tetranychus mcdanieli McGregor (Acarina: Tetranychidea) and Stethorus punctillum Weise (Coleoptera: Coccinellidae) on red raspberry (Rubus idaeus L.), Sitotroga cereallela (Olivier) (Lepidoptera: Gelechiidae) on corn (Zea mays L.), and Halyomorpha halys (Stal) (Hemiptera: Pentatomidae) on green beans [Vigna radiata (L.) Wilczek] (Roy et al. 2003; Hansen et al. 2004; Nielsen et al. 2008). High r2 values were used to choose the Lactin-2 model for T. mcdanieli and the Brière-1 model for S. punctillum, S. cereallela, and H. hays. In the present study, the Wang-Lan-Ding model provided the best fit between temperature and r based on r2 and RSS. However, Angilletta Jr (2006) reported that the selection of model based on r2 and RSS can be erroneous to select the best model. Based on AICC values, the Brière-1 model was the best to describe the relationship between r and temperature. Shi and Ge (2010) also reported the Brière-1, Brière-2 and Performance models to be the most suitable for explaining temperature-dependent development rates of insects. Additional factors such as soil moisture and natural enemies have been reported to affect E. lignosellus populations under field conditions. For example, elevated moisture levels at the soil surface play an important role in reducing oviposition and larval survival under field conditions (Smith & Ota 2002). Larval parasitoids and predators may also play an important role in regulating E. lignosellus population growth in sugarcane (Falloon 1974).

CONCLUSION

Life table analyses determined that the lesser cornstalk borer has the potential to quickly increase its population in sugarcane. Temperatures in the range of 27 to 33 °C were most favorable for reproduction and survival. The results of this temperature-dependent study on reproduction and estimation of life table parameters provides important information that may ultimately be used for predicting outbreaks of the lesser cornstalk borer and improving its management in sugarcane. This data in combination with population monitoring of E. lignosellus under field conditions can be effectively used in population predictions of this pest in the field and severe damage can be prevented by timely implementation of control measures. Additional information is necessary to be able to predict E. lignosellus populations in the field, including relationships among air temperatures and temperatures inside the shoots and in the soil where larvae feed, and the relative attractiveness of stockinette material versus plant tissue and the soil surface for oviposition. Models in this study require field testing before they can reach their full potential for predicting the population dynamics of the lesser cornstalk borer.

ACKNOWLEDGEMENTS

The authors want to thank Drs. J. L. Capinera [Entomology and Nematology Department, University of Florida (UF), Gainesville, FL] and K. Pernezny (EREC, Belle Glade, FL) for providing laboratory facilities for diet preparation. N. Larsen and B. Thappa (EREC, Belle Glade, FL) assisted in collecting adult E. lignosellus to establish the insect colony. Statistical assistance was provided by M. Brennan and J. Colee (Statistics department, UF, Gainesville, FL), and Drs. M. Josan and T. Lang (EREC, Belle Glade, FL). Sandeep Sandhu was instrumental in experimental set up and support. Our sincere thanks to Dr. Peijian Shi (Institute of Zoology, Chinese Academy of Sciences, Beijing) for helping us to calculate parameters for non-linear models. Support funding and land for collecting insects and sugarcane, were provided by the Sugar Cane Growers Cooperative of Florida and the United States Sugar Corporation. This work was made possible by student financial support from the Wedgworth Graduate Fellowship and the University of Florida College of Liberal Arts and Sciences. Publication of this article was funded in part by the University of Florida Open-Access Publishing Fund.

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Hardev S. Sandhu, Gregg S. Nuessly, Susan E. Webb, Ronald H. Cherry, and Robert A. Gilbert "Temperature-Dependent Reproductive and Life Table Parameters of Elasmopalpus lignosellus (Lepidoptera: Pyralidae) on Sugarcane," Florida Entomologist 96(2), 380-390, (1 June 2013). https://doi.org/10.1653/024.096.0258
Published: 1 June 2013
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