basis of the geographic distribution, plant host species, and life-history strategies ... maize (Zea mays L.) from the southern United States to Argentina (Nault & Knoke, 1981; .... rate; gross reproductive rate (G), expected number of eggs laid by a hypothetical female ..... Londres 40, Aparatado Postal 6-641, 06600 Mexico.
475
Ann. a p p l . Biol. (1986), 108, 475-485
Printed in Great Britain
Effect of temperature on the population dynamics of three Dalbulus leafhopper species BY L. V. MADDEN, L. R. NAULT, S. E. HEADY A N D W. E. STYER Departments of Plant Pathology and Entomology. The Ohio State University, Ohio Agricultural Research and Development Center, Wooster, Ohio 44691, USA (Accepted 14 October 1985) SUMMARY
Adult survival and fecundity of three Dalbulus leafhopper species were determined at constant temperatures of 20, 23, 26 and 29°C. Survival was measured by quartiles (i.e. time to 75%, 50% and 25% survival) and estimated parameters of the Weibull model fitted to the survival distributions. D. gelbus lived as long or significantly ( P = 0.05) longer than the other species a t all temperatures. D. maidis (the corn leafhopper) had survival times equal to or significantly shorter than D. elimatus (the Mexican corn leafhopper) at all temperatures except 2 9 ° C where D. maidis lived the longest. The shape of the survival curves did not vary among species or change with temperature. The fecundity of D. gelbus, as measured by the average number of eggs laid per female per generation, was equal to or significantly lower than the other species at all temperatures. D. maidis and D. elimatus had similar fecundity at all temperatures except 29"C, where D. maidis produced significantly more eggs. The mean development time from egg to adult declined with temperature between 17 and 29°C. At all temperatures, D. maidis developed the fastest, D. gelbus the slowest, and D. elimatus was intermediate. The results can be explained on the basis of the geographic distribution, plant host species, and life-history strategies of the leafhoppers. Models for describing the population dynamics of leafhoppers are evaluated and discussed.
INTRODUCTION
The corn leafhopper, Dalbulus maidis (DeLong & Wolcott) occurs in high populations on maize (Zea mays L.) from the southern United States to Argentina (Nault & Knoke, 1981; Oman, 1948). Although common at all altitudes, it is most numerous below 750 m (Barnes, 1954). D. maidis, as well as other Dalbulus spp., has probably had a long evolutionary history with maize, teosinte (Zea spp.), and gamagrass (Tripsacum spp.) (Nault, 1983a, 1983b, 1985; Nault & DeLong, 1980). Nault (1983b, 1985) believes that Dalbulus spp. originated in Mexico where Zea and Tripsacum evolved. There are 10 species of Dalbulus recognised in Mexico, Guatemala, and Costa Rica, and one in Colombia. These include six that were discovered since 1980 (Nault & DeLong, 1980; Nault et al., 1983; Nault, 1985; Triplehorn & Nault, 1985). D . elimatus Ball, the Mexican corn leafhopper, is also common on maize in Mexico, but mainly at altitudes above 750 m (Barnes, 1954). I t also occurs in the southwestern United States (Barnes, 1954), but reports of its occurrence in Central America, where the closely related D. Iongulus DeLong has been discovered, are likely erroneous (Nault, 1985; Triplehorn & Nault, 1985). Both D. maidis and D. elimatus are Zea specialists, rarely occurring on Tripsacum. D. gelbus DeLong is 0 1986 Association of Applied Biologists
476
L . V . M A D D E N , L . R. N A U L T , S . E. H E A D Y A N D W . E. S T Y E R
another high altitude species in Mexico. It may be more common on Tripsacum than on Zea spp., although it frequently has been collected from maize (Nault, 1983a; Nault et al., 1983). Although D. maidis can be a direct pest of maize (Bushing & Burton, 1974), the principal importance of this and other Dalbulus spp. is their ability to transmit the maize stunting pathogens. All Dalbulus spp. tested can transmit the corn stunt spiroplasma (CSS), maize bushy stunt mycoplasma (MBSM), and maize rayado fino virus. All species, however, are not equally efficient as vectors (Nault, Gingery & Gordon, 1980; Madden & Nault, 1983; Nault et al., 1984). Because of its wide geographic distribution, D. maidis is the most important vector of these mollicutes and virus outside Mexico. In Mexico, all Dalbulus spp. that feed on maize are potential vectors. Prior to our investigations, little or nothing was known about the population dynamics of Dalbulus spp. nor the relative importance of these species in transmitting the mollicutes of maize. Knowledge of their population dynamics would help explain their geographic distributions and determine their potential as maize pests and vectors of the stunting pathogens. The present study was conducted: 1) to characterise and compare adult survival, fecundity and egg to adult development times of D. maidis, D. elimatus, and D. gelbus on maize; and 2) to evaluate statistical models for describing leafhopper survival and fecundity. The study was conducted at a range of temperatures typical of low to high altitudes in Mexico.
MATERIALS AND METHODS
Colonies of Dalbulus maidis, D. elimatus, and D. gelbus were maintained in separate 30.5 X 30.5 X 18 cm cages (D'Arcy & Nault, 1982) in a rearing room at c. 26°C with 16 h of light per day. Cages contained six maize seedlings (cv. Aristogold Bantam Evergreen), some of which were replaced weekly with plants at the six-leaf stage. Colonies of the three Dalbulus species were established from specimens collected in Mexico (Madden & Nault, 1983). Experiment I To determine the effect of temperature on the three species, 60 4th-5th instar nymphs or emerging adults (30 males and 30 females) of each species were transferred to separate cages (30.5 X 15 X 18 cm) containing two maize plants at c. the six-leaf stage. The cages were placed in plant growth chambers set at 20,23,26 or 29°C. This was part of a larger experiment in which the effect of CSS and MBSM on D. maidis was evaluated (Madden, Nault, Heady & Styer, 1984). Surviving male and female leafhoppers were counted each week and placed in cages with new maize plants. Eggs in maize leaves during each week were counted under 12X magnification and sub-lighting by a fibre optics probe (Intralux 5000). Three replications (cages) were used and the experiment was terminated when two or fewer females remained alive. Experiment 2 In a separate experiment, 100 adults (50 males and 50 females) of each species were taken from the rearing cages and transferred to separate cages (30.5 X 30.5 X 18 cm) containing six maize plants at c. the six-leaf stage. The cages were kept for 2 days in a chamber set at 26"C, while the leafhoppers mated and oviposited, and then all adults were removed. Three cages were then placed in growth chambers set a t 17,20,23,26,29 or 32°C and were checked periodically for the emergence of adults that developed from eggs deposited earlier by females. Once the first adults were observed at each temperature, the number and sex of those emerging were determined daily until emergence ceased. Development time from egg to adult was previously assessed for eight Dalbulus spp. at a single temperature (Nault & Madden, 1985).
Eflect of temperature on Dalbulus leafhoppers
477
Analysis Survival and fecundity tables were calculated for each species, temperature, and replication in the first experiment. Quartiles, i.e. time from adult emergence to 75% ( t ~ ~50% ) , (?so) and 25% ( f 2 5 ) survival, were determined for each leafhopper survival distribution. The survival distribution is the proportion of leafhoppers alive at any time t . The Weibull model was fitted to the survival distributions using a maximum likelihood procedure (Madden & Nault, 1983). The model can be written as: S ( t ) = exp(-(t/b)')
(1)
in which: S ( t ) is the probability that a leafhopper lives a t least to time t and is equivalent, with our data, to the proportion alive at any time t ; exp( .) is e (2.718 ...) raised to a specified power; b is a scale parameter that is inversely related to death rate; and c is a shape parameter that allows the model to represent survival distributions of many different forms (Lawless, 1982; Madden & Nault, 1983; Madden, 1985). The scale parameter, coincidentally, equals the time to 37% (lOO/e) survival. Fecundity was determined as the number of eggs per adult female per week. Several reproduction statistics were calculated: net reproductive rate (Ro), average number of eggs laid per female per generation; intrinsic rate of natural increase (r,,,),birth rate minus death rate; gross reproductive rate (G), expected number of eggs laid by a hypothetical female leafhopper which lived until the last individual of the cohort died (i.e. no mortality); and the cohort generation time ( T J , mean adult age of egg-laying females. Methods for calculating these statistics have been described elsewhere (Madden, 1985; Pielou, 1977; Southwood, 1978). The Richards model was fitted to the fecundity data using a nonlinear regression technique (Dixon, 1983). The model is of the form: N ( t ) = G(l
+ Be+)'/('-")
(2)
in which: N ( t ) is the cumulative number of eggs laid until time t ; G is the maximum number of eggs laid by a female leafhopper and was set equal to the gross reproductive rate (see above); B is a location parameter that adjusts the fecundity curve along the time axis; k is a rate parameter; and m is a shape parameter analogous to c of the Weibull model. The rate parameter is a measure of the compactness of the fecundity data along the time axis; i.e. a leafhopper species that spreads its egg laying over a wide time interval will have a lower k than a species that lays its eggs over a shorter time period. Values of k cannot be directly compared when G or m differ. Therefore, a derived parameter, the weighted mean fecundity rate (k' = Gk/[2m+2]), is used for comparisons (Richards, 1959; Madden, 1985). The location parameter is positive when m > I and negative when m (1. It is thus inappropriate to compare B values of the Richards model when m is not constant. The survival and fecundity experiment consisted of a randomised factorial with main effect$ of replication, species, and temperature. Variables analysed were: t7&,z , ~t,,, , b, c, R,, r,, G , T,, m and k'. Analysis of variance (ANOVA) was used to determine the significance of main effects and their interactions. A significant species X temperature interaction indicates that, even when a main effect was not significant, species differences were not the same at each temperature or that the change in a variable with temperature was not the same for each species, Unless indicated otherwise, all differences mentioned in the text are significant a t P = 0-05. The egg to adult development time experiment consisted of a randomised factorial with main effects of species and temperature. The mean time of adult emergence (eclosion) was analysed with ANOVA; the interaction was assessed with Tukey's test for additivity and with regression analysis (Neter & Wasserman, 1974). The logarithm of the ratio of male to female
47 8
L V . M A D D E N , L . R . N A U L T , S . E . H E A D Y A N D W . E. S T Y E R
-
-
D. maidis
0
5
10
15
~
I
1
20
25
D._ elimaius
~. ._D.gelhus _
I
L
1
L
Time (wk) Fig. la-h. Adult survival (proportions alive at each week) ( a d ) and fecundity (number of eggs per adult female per week) (e-h) of three Dalbuhs spp. at four temperatures. Curves represent the mean of three replications. Adult eclosion at time 0.
emerging adults was analysed with ANOVA to determine if there were differences in numbers of emerging males and females and also to determine if temperature or species influence the sex ratio.
Efect of temperature on Dalbulus leafloppers
479
Orthogonal polynomials were utilised to determine linear, quadratic, or cubic changes in the variables with respect to temperature. Quadratic and cubic effects reflect curvature to the relationship between variables and temperature.
RESULTS
Experiment 1 Average survival distributions for the three species were similar a t each temperature; however, the rate of population decline and order of the species changed with increasing temperatures (Fig. la-d). There was a significant linear decline in t 7 5 with temperature but species effects and the interaction were not significant. This was probably too soon for species differences to be measured. There were differences among the three species in t5o and 225, although the differences were not the same at each temperature. Survival of these species was nearly the same at 20°C (Fig. 2a, b ) . D. maidis had the shortest survival times at 23 and 26°C but the longest times at 29°C. In general, D. gelbus survival times were greater than or equal to those of the other species. At most temperatures, D. elimatus survival times were intermediate between the other two species. The Weibull model provided good fits to the survival data, as indicated by KolmogorovSmirnov tests (Gibbons, 1976). There was no effect of species, temperature, or their interaction on the Weibull c values (Fig. 2 4 . The overall mean shape parameter equalled 1.65. There were differences in Weibull b (scale parameter) values among the species, which also varied with temperature (Fig. 2c). Results were similar to those obtained when analysing t 2 5 . There were significant interactions between species and the linear, quadratic, or cubic effects of temperature for tso, t 2 5 , and b (Fig. 20-c). The interactions indicate that the change in these variables with time was not the same for each species. Egg laying continued for over 20 or more weeks at the lowest temperature studied but was limited to 10-15 wk at the highest temperature (Fig. le-h). The maximum number of eggs/week increased as the duration of egg-laying decreased. There was a species X temperature interaction for both R, and T, The change in these variables with temperature, therefore, depended on the species (Fig. 3a, d ) . At 2 0 ° C there were no differences in R, between D. maidis and D. elimatus (Fig. 3a); that of D. gelbus was less than D. maidis at this temperature. There were no differences in R, of the three species at the intermediate temperatures of 23 or 26"C, but at 29"C, that of D. maidis was larger than that of the other two species. D. maidis had the shortest T, a t the two lowest temperatures but the longest at 29°C (Fig. 3d). The intrinsic rate of increase only varied in a linear fashion with temperature (Fig. 3c), with no significant species differences. In contrast, there was no effect of temperature on G; the species effect alone was significant and each Dalbulus species was different from the others (Fig. 3b). The Richards model provided excellent fits to the cumulative egg numbers for all species, temperatures, and replications. Coefficients of determination were always greater than 0.95 and usually greater than 0.99. Average estimated parameters are plotted in Fig. 4. G was estimated directly from the data (see Fig. 36), and least squares regression, therefore, was not used for this parameter. Because the shape parameter, m, varied with species (Fig. 4a), it was not possible to directly compare values of k. Analysis of k' indicated that differences of species depended on temperature (Fig. 46). There were little or no differences among the species at 20°C or 23°C. D. maidis had the highest k' at 26"C, and D. elimatus at 29°C. Thus, egg laying by D. maidis was more time-compact than D. elimatus at the former temperatures, whereas the opposite was true at the latter temperature. The interaction of species and the linear and quadratic temperature effects were significant, indicating that,
L. V . M A D D E N , L. R . N A U L T , S. E . H E A D Y A N D W . E. S T Y E R
480
0 D. maidis
0 D. elimalus
I
I
23
I5
26
23
29
26
29
-
-
13-
-m
11-
Y
A D. gelbus
3
v
.-
2
2
s CI
91I
1
I
Temperature ("C) Fig. 2a-d. Effect of temperature on the time in weeks to 50% (IJ and 25% ( I ~ survival, ~ ) and estimated Weibull scale ( b ) and shape (c) parameters of the survival distribution of adult Dalbtrlus maidis, D. elimatus, and D. gelbus leafhoppers. Bars represent S.E.D.'S with 22 D.F. There was no significant (P=0.05) effect of temperature or species on c. Numbers in parentheses preceded by an 'x' indicate which interactions of species and the linear (xl), quadratic (x2). or cubic (x3) orthogonal polynomials of temperature are significant at P=0.05.
although there was a curving increase in k' with temperature, the increase was not the same for each species. Experiment 2 Equal numbers of males and females emerged. Temperature or species did not affect the ratio of males to females. Adults of the three species emerged at all temperatures except at 32"C, where only D. maidis and a few D. elimatus adults were observed. The highest temperature, therefore, was not included in the analysis. ANOVA indicated significant linear, quadratic and cubic declines in mean time to adult emergence with temperature (Fig. 5). ANOVA also indicated a significant effect of species, with D. maidis having the shortest time, D. elirnatus intermediate and D. gelbus the longest time. There was no interaction of species and temperature. The mean emergence time of D. maidis at 32°C was 20 days. DISCUSSION
In nature, D. maidis and D. elimatus primarily utilise maize and related teosinte species for feeding and reproduction (Nault, 1983a, 19836). D. gelbus, on the other hand, although capable of surviving and reproducing on maize in the field and laboratory, is commonly found
Efect of temperature on Dalbulus leafhoppers 0 D. maidis
d 600
c
0 D. elimarus
48 I A D. gelbus
P
(XI, x2, x3)
20
23
26
29
I
I
I
20
23
26
29
tbt
/ a p I I
I
I
23
26
29
Temperature ( " C ) Fig. 3a-d. Effect of temperature on net reproductive rate (R,), gross reproductive rate (G), intrinsic rate of increase (r,,,). and cohort generation time (T,) of Dalbulus maidis, D. elimatus, and D. gelbus leafhoppers. Bars represent S.E.D.'S with 22 D.F.Temperature, species, and their interaction were significant for R, and T, (P=0.05). Only species was significant for G and temperature for r,,, ( P 0 . 0 5 ) . G values of the three species averaged across temperatures were significantly different from each other. Numbers in parentheses indicate which orthogonal polynomials of temperature are significant at b 0 . 0 5 (i.e. 1, 2, and 3 indicate linear, quadratic, and cubic effects). Numbers preceded by an 'x' indicate that the interaction of temperature and species is significant.
on gamagrasses in nature, of which all are perennials. Based on the relative permanence of the perennial habitat, Nault & Madden (1985) predicted that leafhopper species which specialise on annual plants will develop more rapidly, reproduce earlier, but not live as long as species that specialise on perennials. Using the terminology of MacArthur & Wilson (1967) as presented by Southwood (1977), D. maidis and D. elimatus can be considered r-strategists relative to D. gelbus, an intermediate in an r-K continuum among Dalbulus spp. Development time of D. gelbus from egg to adult was slower than the other two species (Fig. 5). This agreed with another study at a single temperature in which development was assessed on maize and the perennial, Tripsacum dactyloides L. (Nault & Madden, 1985). Development was faster on maize than on T. dactyloides. Adult survival was as long or longer than the others at all temperatures tested (Fig. 2). It had the lowest gross reproductive rate, and had a net reproductive rate and weighted mean fecundity rate as low or lower than the other species at all temperatures (Fig. 3). Except at 29"C, the mean age of egg-laying adults was greater than or equal to the other species.
482
L . V . M A D D E N . L . R . N A U L T , S . E. H E A D Y A N D W . E. S T Y E R
0 D. elirnalus
0 D. maidis
A D. gelbus
-(
F
1.5-
I
-5.0
.o-
20
23
26
29
Temperature ("C) Fig. 4a-b. Effect of temperature on the estimates of rn and k' of the Richards model fitted to the cumulative number of eggs produced by Dalbulus maidis, D. elimafus,and D. gelbus leafhoppers. Bars represent S.E.D.'S with 22 D.F. Only the main effect of species was significant for m. X I and x 2 on the plot of k' indicates that there was a significant (P=O.O5) interaction of species and the linear and quadratic orthogonal polynomials of temperature.
Compared to D. gelbus, D. maidis and D. elimatus have the population dynamic characteristics of r-strategists. Differences between these two species were, for the most part, dependent on temperature. Only with G and development time were the differences consistent at all temperatures; D. maidis had a larger G and faster development time than D. elimatus (Figs 36, 5 ) . At 20"C, there was no difference in survival times or fecundity, as measured by R, and k' between the two (Figs 3a, 46). At the intermediate temperatures of 23 and 26"C, D. maidis had a survival time equal to or shorter than D. elimatus. Fecundity of the two species also was similar at these temperatures. At the highest temperature studied (29"C),D. maidis lived longest, had the highest T,, and the highest fecundity (Figs 2a-c, 3a, d ) . The geographic distribution of these two species is consistent with our results. Although their distributions overlap, D. maidis is found in greatest numbers in the lower altitudes (Neotropical regions) of Mexico where mean daily summer temperatures of 27°C or higher occur (Barnes, 1954; Sperling, 1984). D. elimatus is mainly found at higher elevations (Nearctic regions) where mean daily summer temperatures near 20°C or lower prevail. Although both species survived and reproduced readily at all temperatures tested, D. maidis was clearly better adapted to 29°C. D. elimatus thus may be outcompeted by D. maidis at lower elevations in Mexico where temperatures are higher. There is little difference in the population dynamics of the two species a t temperatures lower than 29°C. The fewer D. maidis leafhoppers found at high elevations in Mexico may be due to other factors. Little is known about overwintering or the natural parasites and predators of the leafhoppers in this genus (Nault, 1985). The mollicutes causing stunting diseases of maize (CSS and MBSM) may affect the geographic distribution of these three Dalbulus spp. In addition to being plant pathogens, these two mollicutes are differentially pathogenic to their vectors. CSS is pathogenic to all Dalbulus spp. except D. maidis (Madden & Nault, 1983; Madden et al., 1984; Nault et al., 1984),and both CSS and D. maidis have a Neotropical distribution in Mexico (Nault, 1983b). MBSM is pathogenic to all species except D. elimatus and D. gelbus, and both the leafhoppers and the mollicute have a Nearctic distribution in Mexico. The Weibull model accurately represented leafhopper survival. By using the estimated values of b and c, one can determine the probability of a leafhopper surviving until a given time t by using equation 1. In addition to providing an empirical description of survival curves,
EHect of temperature on Dalbulus leajhoppers
48 3
c
75
0 D.maidis 0 D. elimarus A D. gelbus
I
1
I
I
20
23
26
29
Temperature ( " C ) Fig. 5 . Effect of temperature on the mean time from egg to adult eclosion for Dalbulus maidis, D. elimatus, and D. gelbus. Bar represents the S.E.D with 8 D.F. There were linear, quadratic, and cubic changes in the means with temperature (P=0.05). The three species were significantly different from each other.
the Weibull model can be rationalised based on hazard rates. The hazard rate [ h ( t ) ] is the instantaneous death rate at t given survival until t . The hazard rate multiplied by a small increment of time (A t ) is equal to the probability of dying in the interval ( t A t ) given survival until t . Hazard rates generally are analysed in detail with survival analysis in many disciplines (Lawless, 1982). Indeed, Rowel1 & Markham (1 984) analysed leafhopper survival using hazard rates. The hazard rate of many organisms can be written as:
+
h ( t ) = Pt'
(3)
in which p and y are parameters. When y equals 0, h ( t ) equals a constant value of p. When y >0, h ( t ) increases over time if is positive; the increase is linear when y = 1. If y to, h ( t ) declines over time. Equation 3 cannot represent hazard rates that increase to a maximum and then decline. Both parameters of equation 3 control the value of h ( t ) at any time. Slight changes in y have a greater effect on h ( t ) than changes in p. Biotic and abiotic factors influence the values of the parameters. The hazard rate of the Weibull model can be written as a form of equation 3: h ( t ) = cb-c ( t c - ' ) (4)
in which p = cb-c and y = c-I. Equation 4 is equivalent to equation 3 in Madden & Nault (1983). Larger values of b lead to smaller values of p. Temperature did not affect the estimated shape parameter of any species, nor were there significant differences among the three Dafbuius spp. (Fig. 2 4 . The estimated value of c indicated that h ( t ) of these leafhoppers increased over time. This agrees with results reported
484
L . V . M A D D E N , L . R . N A U L T , S . E . H E A D Y A N D W . E. STYER
previously for seven Dalbulus spp. at 26°C (Madden & Nault, 1983). The estimates of c were somewhat lower in this study than in Madden & Nault (1983), probably due to the larger number of leafhoppers used in this study resulting in more precise parameter estimates. Although not found here, c can vary among leafhopper cohorts. For instance, acquisition of CSS by D. gelbus resulted in an increased c compared to the control (Madden & Nault, 1983; Madden et al., 1984). Temperature had a less drastic effect on hazard rates than did certain mollicute exposures. Only the estimates of b (or 0) varied with temperature and differences in b among species depended on temperature (Fig. 2c). We are continuing to study the hazard rates of leafhoppers to determine: i) the generality of equation 3 (or 4); ii) the relationship between equation 4 and the four basic types of survival curves (Southwood, 1978); and iii) when equation 4 is appropriate, the factors which directly influence b or c or both. The Weibull model has accurately fitted survival (and hazard rate) data of seven Dalbulus spp., Baldulus tripsaci Kramer & Whitcomb, and Graminella nigrifrons (Forbes) (Madden & Nault, 1983; Madden el al., 1984; Nault et al., 1984; L. V. Madden, unpublished). In preliminary analyses of data reported by Rowel1 & Markham (1984), however, the hazard rate of Euscelidius variegatus (Kirsch.) was not accurately represented by equation 3 (or 4). The hazard rate increased to a maximum and then declined; the log-normal model better fitted their data than did the Weibull model based on likelihood ratio test (L. V. Madden, unpublished). The Richards model was found to accurately represent fecundity data of the three Dalbulus spp. at four temperatures. Unlike R, and rm, parameters of this model permit the analysis of fecundity independent of survival. As indicated by G (Fig. 3b), a female leafhopper of a given species which lived until all individuals in a cohort were dead, would produce the same total number of eggs at all tested temperatures. Species differences for G were the same at all temperatures. Temperature did, however, affect the rate of egg production ( k ' ) and differences of k' among species. The differential effect of temperature on k', together with survival differences among the three species, resulted in differences in R, among the species that depended on temperature. There has been relatively little effort in studying the population dynamics of leafhoppers (Madden, 1985). This is surprising considering the many economically important species involved. However, the work described herein on the use of the Weibull and Richards models, as well as previously developed life and fecundity analyses (Southwood, 1978), are general enough to .be applicable to many leafhopper species. Analyses of this type are useful to compare species, evaluate treatments, and ultimately predict leafhopper numbers. Salaries and research support were provided by State and Federal funds (especially USDA Competitive Grant No. 84-CRCR-1 - 1370) appropriated to the Ohio Agricultural Research and Development Center, The Ohio State University. Journal Article No. 6-85. We thank E. Benekos, G. Homany, K. Keller, S. S . Mendiola, and B. Ogden for technical assistance. REFERENCES
(1954). Biologia ecologia y distribucibn de las chicharritas, Dalbulus elimatus (Ball) y Dalbulus maidis (DeL. & W.).Folleto T2cnico. Ojicina de Estudios Especiales, Secretaria de Agricultura y Canaderia, Mexico DF No. 1 1 . 1 12 pp. BLJSHING, R w , & BURTON. v E (1974). Leafhopper damage to silage corn in California. Journa/ of Economic Entomology 67, 656-658. DARCY. c J . & NAULT. L R (1 982). Insect transmission of plant viruses, mycoplasmalike and rickettsialike organisms. Plant Disease 66, 99-104. DIXON, w J (1983). BMDP Statistical Software. Berkeley: University of California Press. 733 pp. GIBBONS, J D (1976). Nonparametric Methods for Quantitative Analysis. New York: Holt, Rinehart, and Winston. 463 pp. BARNES, D
EHect of temperature on Dal bulus leufloppers
485
(1982). Statistical Models and Methods for Lifetime Data. New York: John Wiley & Sons. 580 pp. MACARTHUR, R. H. & WILSON. E. 0.(1967). The Theory of Island Biography. Princeton: Princeton University Press, New Jersey. 203 pp. MADDEN, L. v. (1985). Modeling the population dynamics of leafhoppers. In The Leafloppers and Planthoppers, pp. 235-238. Eds L. R. Nault and J. G. Rodriquez. New York: John Wiley & Sons. MADDEN, L. v. & NAULT. L. R . (1983). Differential pathogenicity of corn stunting moilicutes to leafhopper vectors in Dalbulus and Baldulus species. Phytopathology 73, 1608-1614. MADDEN, L. v., NAULT. L. R., HEADY, s. E., ~r STYER, W. E. (1984). Effect of maize stunting mollicutes on survival and fecundity of Dalbulus leafhopper vectors. Annals of Applied Biology 105, 431-441. NAULT, L. R. (1983a). Origins in Mesoamerica of maize viruses and mycoplasmas and their leaflopper vectors. In Plant Virus Epidemiology, pp. 259-266. Eds R. T. Plumb and J. M. Thresh. Oxford: Blackwell Scientific Publications. NAULT, L. R. (19838). Origins of leafhopper vectors of maize pathogens in Mesoamerica. In Proceedings International Maize Virus Disease Colloquium and Workshop, 2-6 August 1982, pp. 75-82. Eds D. T. Gordon, J. K. Knoke, L. R. Nault and R. M. Ritter. Wooster: The Ohio State University, Ohio Agricultural Research and Development Center. NAULT, L. R. (1985). Evolutionary relationships between maize leafhoppers and their host plants. In The Leapoppers and Planthoppers, pp. 309-330. Eds L. R. Nault and J. G. Rodriquez. New York: John Wiley & Sons. NAULT, L. R. & DELONG, D. M. (1980). Evidence for co-evolution of leafhoppers in the genus Dalbulus (Cicadellidae: Homoptera) with maize and its ancestors. Annals of the Entomological Society of America 73, 349-353. NAULT, L. R., DELONG, D. M., TRIPLEHORN, B. W.. STYER, W. E., & DOEBLEY. J. F. (1983). More on the association of Dalbulus (Homoptera: Cicadellidae) with Mexican Tripsacum (Poaceae) including the description of two new species of leafhoppers. Annals of the Entomological Society of America 76, 305-309. NAULT. L. R.. GINGERY, R. E., & GORDON, D. T. (1980). Leafhopper transmission and host range of maize rayado fino virus. Phytopathology 70, 709-7 12. NAULT. L. R., & KNOKE, J. K. (1981). Maize vectors. In Virus and Viruslike Diseases of Maize in the United States, pp 77-84. Eds D. T. Gordon, J. K. Knoke, and G . E. Scott. Ohio: Ohio Agricultural Research and Development Center, Wooster. NAULT. L. R. & MADDEN, L. v. (1985). Ecological strategies of Dalbulus leafhoppers. Ecological Entomology 10, 57-63. NAULT, L. R., MADDEN, L. V.,STYER, W. E.,TRIPLEHORN, B. W.,SHAMBAUGH,G. F., & HEADY,S. E. ( 1 984). Pathogenicity of corn stunt spiroplasma and maize bushy stunt mycoplasma to its vector Dalbulus longulus. Phytopathology 74, 977-919. NETER. J. & WASSERMAN, W. (1974). Applied Linear Statistical Models. Homewood: Richard D. Irwin Inc., Illinois. 842 pp. OMAN, P. w. (1948). Distribution of Baldulus maidis (DeLong & Wolcott). Proceedings Entomological Society of Washington 50, 34. PIELOU. E. C. (1977). Mathematical Ecology. New York: Wiley Interscience. 385 pp. RICHARDS, F. J. (1959). A flexible growth function for empirical use. Journal of Experimental Botany 10, 290-300. ROWELL, J. G., & MARKHAM. P. G. (1 984). Modelling mortality risks for treated insects relative to controls. Annals of Applied Biology 105, 15-27. SOUTHWOOD, T. R. E. (1977). Habitat, the template for ecological strategies. Journal of Animal Ecology 46, 337-365. SOUTHWOOD, T. R. E. (1978). Ecological Methods, 2nd Ed. London: Chapman and Hall. 524 pp. SPERLING, D. w. (1984). Compendium of selected meteorological data for the El Batan. Poza Rica, Tlaltizapan and Toluca experiment stations. Centro Internacional de Mejoramiento de Maiz y Trigo. Londres 40, Aparatado Postal 6-641, 06600 Mexico. 94 pp. TRIPLEHORN,B. w. & NAULT, L. R. (1985). Phylogenetic classification of the genus Dalbulus (Homoptera: Cicadellidae), and notes on the phylogeny of the Macrostelini. Annals of the Entornological Society of America 78, 291-315. LAWLESS, J. F.
(Received 9 January 1985)
