Influence of Latitude and Elevation on Polymorphism Among ...

PHYSIOLOGICAL ECOLOGY

Influence of Latitude and Elevation on Polymorphism Among Populations of the Corn Leafhopper, Dalbulus maidis (DeLong and Wolcott) (Hemiptera: Cicadellidae), in Brazil CHARLES MARTINS DE OLIVEIRA,1 JOAÕ ROBERTO SPOTTI LOPES,2 CARLOS TADEU DOS SANTOS DIAS,2 AND LOWELL R. NAULT3 Departamento de Entomologia, Fitopatologia e Zoologia Agrõćola, Escola Superior de Agricultura “Luiz de Queiroz,” Universidade de Saõ Paulo, C. Postal 9, Piracicaba, SP 13418-900, Brazil

Environ. Entomol. 33(5): 1192Ð1199 (2004)

ABSTRACT Morphological variations in insects have been shown to be inßuenced by latitude and elevation. Here we show that these two parameters markedly inßuence the appearance of the corn leafhopper Dalbulus maidis (DeLong and Wolcott). Leafhopper samples were collected in maize from 27 localities in 10 Brazilian states, with latitudes from 5 to 28⬚ S and elevations from 16 to 1,628 m. D. maidis was the only Dalbulus species found in the samples. Up to 10 males and 10 females of D. maidis from each collection site were evaluated for size, pigmentation, and body weight. Females were always bigger and heavier than the males in the same locality. For both sexes, there was a positive and signiÞcant correlation between the morphological variables measured and the latitude and elevation from where specimens were collected. Individuals from higher latitudes (southern region) were bigger, darker, and heavier than those from lower latitudes (northeastern region). There was also a tendency for an increase in body weight, head capsule width, and wing length at higher elevations. RESUMO Variaç o˜ es morfolo´ gicas em insetos podem ser inßuenciadas por latitude e elevaç aõ. Neste estudo no´ s mostraˆmos que esses dois paraˆmetros inßuenciam marcadamente a apareˆ ncia da cigarrinhado-milho, Dalbulus maidis (DeLong and Wolcott). Cigarrinhas foram coletadas em milho em 27 localidades de 10 Estados brasileiros, com latitudes de 5 a 28⬚S e elevaç o˜ es de 16 a 1.628 m. D. maidis foi a u´ nica espe´ cie de Dalbulus encontrada nas amostras. Examinaram-LC 10 machos e 10 feˆ meas de D. maidis de cada local de coleta, quanto ao tamanho, pigmentaç aõ e peso do corpo. Feˆ meas foram sempre maiores e mais pesadas que os machos em uma mesma localidade. Para ambos os sexos, houve uma correlaç aõ positiva e signiÞcativa entre as varia´veis morfolo´ gicas avaliadas e a latitude e elevaç aõ de onde os espe´ cimes foram coletados. Espe´ cimes coletados em latitudes mais altas (regiaõ CentroSul) foram maiores, mais pigmentados e pesados do que aqueles de menores latitudes (regiaõ Nordeste). Houve tambe´ m uma tendeˆ ncia de aumento do peso do corpo, largura da capsula cefa´lica e comprimento da asa em maiores elevaç o˜ es. KEY WORDS insect vector, morphological variation, Zea mays

THE DELTOCEPHALINE LEAFHOPPER GENUS Dalbulus DeLong includes 13 species distributed in the American continent, primarily in Mexico and Guatemala. Leafhopper hosts are the domesticated maize (Zea mays L.), the wild teosintes (Zea spp.), or gammagrasses (Tripsacum spp.) (Nault and Styer 1994). The corn leafhopper, Dalbulus maidis (DeLong and Wolcott), is the most widespread species because of its intimate association with cultivated maize (Triplehorn and 1 Corresponding author: Embrapa Cerrados, C. Postal 08223, Planaltina DF 73310-970, Brazil. E-mail: [email protected]. 2 Escola Superior de Agricultura “Luiz de Queiroz,” Universidade de Saõ Paulo, C. Postal 9, Piracicaba SP 13418-900, Brazil. 3 Department of Entomology, Ohio Agricultural Research and Development Center, The Ohio State University, Wooster, OH 44691.

Nault 1985). This leafhopper is the vector of three pathogens associated with corn stunt disease, the maize rayado Þno maraÞvirus (MRFV), and the mollicutes, Spiroplasma kunkelii Whitcomb (“corn stunt spiroplasma” [CSS]) and maize bushy stunt phytoplasma (MBSP), which are limiting factors to maize production in Latin America (Nault 1990, Oliveira et al. 1998). Dalbulus maidis occurs throughout the neotropics, from the southern United States to northern Argentina (Oman 1948, Triplehorn and Nault 1985). It is the only Dalbulus species recorded on maize in South America. Because the corn leafhopper has such a wide distribution, it would be expected that morphological and physiological variations occur among its populations.

0046-225X/04/1192Ð1199$04.00/0 䉷 2004 Entomological Society of America

October 2004 Table 1. Region Northeast

Central-south

a b

OLIVEIRA ET AL.: POLYMORPHISM AMONG POPULATIONS OF D. maidis

1193

Brazilian localities where leafhoppers were sampled on maize Locality

Abbreviation

Collecting date

Latitude (S)

Elevation (m)

Temperature (⬚C)a

Nb

Ipanguaç u/RN Ceara´-Mirim/RN Lagoa Grande/PE Petrolina/PE Juazeiro/BA Barreiras/BA Brasõ´lia/DF Rio Verde/GO Itumbiara/GO Sete Lagoas/MG Divino´ polis/MG Guaõ´ra/SP Anastaćio/MS Franca/SP Passos/MG Brodowski/SP Bonito/MS Lavras/MG Cravinhos/SP Poç os de Caldas/MG Piracicaba/SP Campos do Jordaõ/SP Jacarezinho/PR Arapongas/PR Toledo/PR Castro/PR Chapeco´ /SC

Ip CM LG Pe Ju Ba Br RV It SL Di Gu Na Fr Pa Bd Bo La Cr PC Pi CJ Ja Ar To Ca Ch

8/19/1996 1/17/1996 1/19/1996 8/23/1996 8/22/1996 5/9/1995 1/10/1996 7/8/1995 5/29/1996 5/19/1995 1/5/1996 11/6/1995 1/4/1996 2/26/1996 3/23/1996 2/27/1996 10/2/1995 1/9/1996 5/12/1995 4/8/1996 3/6/1996 4/3/1996 5/4/1996 3/27/1996 3/12/1996 3/13/1996 12/18/1995

05⬚29⬘54⬙ 05⬚38⬘04⬙ 08⬚59⬘49⬙ 09⬚23⬘55⬙ 09⬚24⬘42⬙ 12⬚09⬘10⬙ 15⬚46⬘47⬙ 17⬚47⬘53⬙ 18⬚25⬘09⬙ 19⬚27⬘57⬙ 20⬚08⬘20⬙ 20⬚19⬘06⬙ 20⬚29⬘01⬙ 20⬚32⬘19⬙ 20⬚43⬘08⬙ 20⬚59⬘29⬙ 21⬚07⬘16⬙ 21⬚14⬘43⬙ 21⬚20⬘25⬙ 21⬚47⬘16⬙ 22⬚43⬘31⬙ 22⬚44⬘22⬙ 23⬚09⬘38⬙ 23⬚25⬘10⬙ 24⬚42⬘49⬙ 24⬚47⬘28⬙ 27⬚05⬘47⬙

16 33 300 376 368 452 1,171 715 448 761 712 517 160 996 745 861 315 919 788 1,196 547 1,628 501 729 560 999 674

27.2 25.4 26.4 26.3 26.3 24.3 21.2 22.5 19.0 20.9 23.0 23.6 21.0 20.1 20.7 20.8 22.0 19.4 21.0 17.0 21.6 14.8 20.3 21.0 19.8 16.2 18.7

180 8 470 207 157 85 4 205 108 333 127 463 5 174 90 117 5 55 128 134 517 88 131 317 257 285 11

Mean annual temperature (Departamento Nacional de Metereologia 1992). Number of individuals sampled in each locality.

These variations likely would help the corn leafhopper cope with varying environmental conditions that occur over its range of distribution from sea level to high mountain elevations (Nault 1990). For example, body weight (size) for D. maidis would likely agree with the rule of Bergmann (1847) rule, which states that weight tends to be at a minimum in warmer regions and increases to a certain threshold as temperature declines. Many insect species vary in size and coloration in response to environmental conditions. This polymorphism aids in dormancy, thermoregulation, reproduction, and other forms of adaptation to seasonal changes in the environment (Tauber et al. 1986). The size and coloration of adult leafhoppers are inßuenced by environmental factors that act on the immatures, such as temperature, photoperiod, and host plant condition (Harrison 1980). Under laboratory conditions, Larsen and Nault (1994) observed increases in size, weight, and pigmentation of adults of Þve Dalbulus species when immatures were reared on mature maize at low temperatures and short day length, typical of late season conditions in Mexico. A similar relationship between rearing temperature and adult morphology has been reported for leafhoppers Empoasca fabae (Harris) (Simonet and Pienkowiski 1980) and Graminella nigrifrons (Forbes) (Larsen et al. 1990). Polymorphism has also been observed along latitudinal and elevational gradients for several insect groups (Cushman et al. 1993, Hawkins and Lawton 1995, Krasnov et al. 1996, Smith et al. 2000). In a previous study, Larsen and Nault (1994) showed that populations of D. maidis from Jalisco,

Mexico, varied in morphology depending on the time of year leafhoppers were collected. Here we show that morphology of the leafhopper varies among populations along a range of latitudes and elevations in Brazil. Materials and Methods Leafhopper Sampling. Leafhoppers were collected in maize Þelds in 27 localities of 10 Brazilian states in latitudes ranging 5Ð28⬚ S and elevations between 16 and 1,628 m (Table 1; Fig. 1). Most samplings were done in the vegetative growth stage of maize (before tasseling), during summer and fall months (DecemberÐJune), except for those in Guaõ´ra/SP and Bonito/ MS, which were carried out in the spring, and Ipanguaç u/RN, Petrolina/PE, and Juazeiro/BA, which were carried out in the winter. Adult leafhoppers were collected from maize whorls with a sweep net or a mouth-operated aspirator. In Sete Lagoas/MG, leafhoppers were also collected from sorghum (Sorghum bicolor L. Moench), Brachiaria sp., and B. plantaginea (Link). Species identiÞcation was performed as described by Triplehorn and Nault (1985). Morphological Evaluation. Ten D. maidis males and 10 females from each locality were randomly selected for measurements of dry weight, pigmentation, and size of selected body parts, according to Larsen and Nault (1994). Through a digital micrometer (Wild MMS 235 display and Wild Typ. 325400 ocular, Wild Heerbrugg Ltd., Heerbrugg, Switzerland) coupled to a stereoscopic microscope, each specimen was measured for the distance between the compound eyes in the head vertex, the length of the second medium cell

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1993). Separately for each sex, a PearsonÕs correlation analysis was performed between each of the morphological variables and the latitude and elevation of the collecting sites, as well as a correlation between the latitude and elevation and the mean annual temperatures of each of the localities. In addition, a canonical correlation analysis (SAS Institute 1993) was performed between the set of morphological and geographic variables (latitude and elevation). The canonical correlation was tested through the same multivariate tests used for the sex comparison. To study clusters of D. maidis populations according to morphological similarity, a cluster analysis by the unweighted pair group method of arithmetic means (unweighted pair-group method with arithmetic average; SAS Institute 1993) was performed by combining all set of morphological variables. Dalbulus maidis voucher specimens were deposited with the Entomology Museum of the Escola Superior de Agricultura “Luiz de Queiroz”/USP, Brazil. Fig. 1. Map showing the collection localities of D. maidis in Brazil. (see Table 1 for abbreviations).

Results

of the fore wings (Larsen et al. 1990), and the length of the ovipositor, from the hollow portion of the seventh sternite to its tip. The intensity of abdomenal pigmentation was evaluated as an indicator of body coloration. Leafhooper wings were removed to expose the back of the abdomen from the third to the Þfth segment. Groups of Þve individuals, separated according to sex, were placed onto a microscopic slide with a small amount of glycerin to keep them in the dorsal position and photographed with a slide Þlm (Fuji RDP II ASA 100, Fuji Photo Film da Amazoˆ nia Ltda, Manaus, AM, Brazil). The slides were projected in a dark room with a Kodak Ektagraphic III projector (85Ð150 mm, Zoom f/3.5, Kodak da Amazoˆ nia Ind. Com. Ltda, Maneus, AM, Brazil) located 3.5 m from the screen. The intensity of the pigmentation of each specimen was indirectly estimated by measuring, at the screen, the light intensity (␮E/s/m) transmitted through the abdomen image. A photometer (model LI-189, LI-COR, Lincoln, NE, USA) equipped with a Quantum-type sensor (LI-190SA; LI-COR, Lincoln, NE) was used to measure light intensity. The darker the abdomen exoskeleton, the less the intensity of transmitted light. After pictures were taken, the wingless specimens were dried for 3 d in an oven at 80⬚C and individually weighed in a 10⫺5 g precision electric scale. Statistical Analysis. The data on leafhopper size (interocular distance, wing, and ovipositor length), pigmentation, and dry weight were analyzed by the Statistical Analysis System V. 6.08 (SAS Institute 1993). For sex comparison, a univariate analysis of variance (ANOVA) of the morphological variables was performed using the number of individuals per sample as a covariate. Also, a multidimensional ANOVA (MANOVA) was performed by using the multivariate tests of WilkÕs Lambda, PillaiÕs Trace, Hotelling-LawleyÕs Trace, and RoyÕs Greatest Root (SAS Institute

Dalbulus maidis was the only species of the genus Dalbulus found in a total of 4,661 individuals sampled from 27 Brazilian localities. D. maidis represented 74% of a total of 1,103 cicadellid specimens collected in 17 localities. D. maidis adults also were collected in sorghum in Sete Lagoas/MG, but less frequently (around 15%) than leafhopper species of other genera. In samples collected in Brachiaria sp. and Brachiaria plantaginea (Link), also from Sete Lagoas/MG, no Dalbulus leafhoppers were found. The morphological analysis showed that D. maidis females are signiÞcantly heavier (F ⫽ 103.5; P ⬍ 0.01; df ⫽ 1,49) and bigger than males, with greater interocular distance (F ⫽ 31.4; P ⬍ 0.01; df ⫽ 1,49) and longer right (F ⫽ 44.0; P ⬍ 0.01; df ⫽ 1,49) and left (F ⫽ 41.2; P ⬍ 0.01; df ⫽ 1,49) wings. No signiÞcant difference was observed between the genders for body pigmentation (F ⫽ 0.9; P ⫽ 0.35; df ⫽ 1,49). When all morphological variables were combined in the multidimensional variance analysis, the gender difference was highly signiÞcant in all four multivariate tests (F ⫽ 30.3; P ⬍ 0.01; df ⫽ 5,45). Regarding length of the fore wings, D. maidis was asymmetric: the length of the left wing was longer than that of the right wing in nearly every collection locality, both for males and females (Tables 2 and 3). The clustering of collecting localities by similarity (cluster analysis), in which all D. maidis morphological variables were combined for each sex, showed two distinct groups: (1) northeast region localities and (2) central-south region localities (Figs. 2 and 3). The only exception was for Barreiras/BA (northeast), which does not belong to group 1 based on data from females (Fig. 2). The Euclidean distance separating these two groups is very large, indicating that the morphological differences between them are highly signiÞcant for females (Fig. 2) and males (Fig. 3). Latitude was the main factor separating the two groups. Group 1 includes localities between the latitudes 05⬚29⬘54⬙ and

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Table 2. Means ⴞ SEM of morphological variables related to body size, weight, and pigmentation of males of D. maidis collected in different Brazilian localities Region Northeast

Central-south

Collecting locality

Dry weight (mg)a

Interocular distance (mm)

Left wing (mm)b

Right wing (mm)b

Light intensity (␮E/s/m2)c

Nd

Ipanguaç u/RN Ceara´-Mirim/RN Lagoa Grande/PE Petrolina/PE Juazeiro/BA Barreiras/BA Brasõ´lia/DF Rio Verde/GO Itumbiara/GO Sete Lagoas/MG Divino´ polis/MG Guaõ´ra/SP Franca/SP Anastaćio/MS Passos/MG Brodowski/SP Lavras/MG Cravinhos/SP Poç os de Caldas/MG Piracicaba/SP Campos do Jordaõ/SP Jacarezinho/PR Arapongas/PR Toledo/PR Castro/PR Chapeco´ /SC

0.18 ⫾ 0.010 0.15 ⫾ 0.004 0.17 ⫾ 0.009 0.19 ⫾ 0.006 0.18 ⫾ 0.004 0.22 ⫾ 0.003 0.23 ⫾ 0.009 0.25 ⫾ 0.010 0.23 ⫾ 0.008 0.26 ⫾ 0.004 0.24 ⫾ 0.008 0.24 ⫾ 0.007 0.29 ⫾ 0.012 0.19 ⫾ 0.007 0.28 ⫾ 0.005 0.29 ⫾ 0.006 0.29 ⫾ 0.008 0.22 ⫾ 0.003 0.29 ⫾ 0.007 0.23 ⫾ 0.005 0.32 ⫾ 0.002 0.24 ⫾ 0.007 0.26 ⫾ 0.003 0.28 ⫾ 0.003 0.31 ⫾ 0.002 0.30 ⫾ 0.006

0.39 ⫾ 0.005 0.37 ⫾ 0.008 0.40 ⫾ 0.005 0.39 ⫾ 0.004 0.41 ⫾ 0.006 0.41 ⫾ 0.042 0.43 ⫾ 0.003 0.44 ⫾ 0.005 0.42 ⫾ 0.005 0.44 ⫾ 0.007 0.45 ⫾ 0.004 0.44 ⫾ 0.007 0.44 ⫾ 0.004 0.45 ⫾ 0.012 0.43 ⫾ 0.004 0.44 ⫾ 0.011 0.45 ⫾ 0.004 0.43 ⫾ 0.030 0.44 ⫾ 0.004 0.43 ⫾ 0.004 0.45 ⫾ 0.004 0.43 ⫾ 0.006 0.43 ⫾ 0.009 0.44 ⫾ 0.004 0.46 ⫾ 0.007 0.50 ⫾ 0.024

1.51 ⫾ 0.018 1.52 ⫾ 0.018 1.54 ⫾ 0.067 1.54 ⫾ 0.021 1.55 ⫾ 0.014 1.53 ⫾ 0.013 1.70 ⫾ 0.015 1.70 ⫾ 0.014 1.63 ⫾ 0.028 1.67 ⫾ 0.017 1.63 ⫾ 0.024 1.65 ⫾ 0.014 1.69 ⫾ 0.028 1.63 ⫾ 0.046 1.72 ⫾ 0.013 1.71 ⫾ 0.032 1.75 ⫾ 0.015 1.65 ⫾ 0.011 1.75 ⫾ 0.026 1.63 ⫾ 0.024 1.70 ⫾ 0.014 1.64 ⫾ 0.016 1.67 ⫾ 0.027 1.70 ⫾ 0.026 1.76 ⫾ 0.022 1.72 ⫾ 0.036

1.51 ⫾ 0.019 1.51 ⫾ 0.017 1.52 ⫾ 0.017 1.50 ⫾ 0.020 1.50 ⫾ 0.015 1.55 ⫾ 0.018 1.69 ⫾ 0.014 1.66 ⫾ 0.013 1.60 ⫾ 0.021 1.65 ⫾ 0.011 1.60 ⫾ 0.021 1.63 ⫾ 0.014 1.65 ⫾ 0.028 1.58 ⫾ 0.070 1.68 ⫾ 0.017 1.67 ⫾ 0.031 1.70 ⫾ 0.019 1.62 ⫾ 0.020 1.69 ⫾ 0.034 1.58 ⫾ 0.020 1.67 ⫾ 0.015 1.63 ⫾ 0.017 1.65 ⫾ 0.013 1.66 ⫾ 0.014 1.73 ⫾ 0.016 1.70 ⫾ 0.036

1.56 ⫾ 0.068 1.19 ⫾ 0.073 1.15 ⫾ 0.135 1.44 ⫾ 0.127 1.32 ⫾ 0.093 1.22 ⫾ 0.122 0.44 ⫾ 0.260 0.88 ⫾ 0.155 0.74 ⫾ 0.136 0.39 ⫾ 0.070 0.73 ⫾ 0.121 0.30 ⫾ 0.032 0.44 ⫾ 0.067 0.88 ⫾ 0.137 0.60 ⫾ 0.109 0.78 ⫾ 0.126 0.53 ⫾ 0.127 0.29 ⫾ 0.049 0.25 ⫾ 0.072 0.49 ⫾ 0.666 0.18 ⫾ 0.024 0.36 ⫾ 0.086 0.39 ⫾ 0.067 0.30 ⫾ 0.054 0.14 ⫾ 0.023 0.83 ⫾ 0.169

10 5 10 10 10 10 3 10 10 10 10 10 10 5 10 10 10 10 10 10 10 10 10 10 10 4

a

Dry body weight (without wings). Winglength, represented by the length of the second median cell of the forewing. Light intensity transmited through the slide picture of the abdomen (lower values indicate darker specimens). d Number of individuals analyzed. b c

09⬚24⬘42⬙ S. Nevertheless, it is important to notice that the elevation in all localities in group 1 is below 400 m. Thus, the lower latitude and lower elevation of the northeast localities might have contributed to the separation of the two groups (Table 1). Several subgroups are observed within group 2 for both genders. Differences in latitude or elevation do not seem to explain the separation of these subgroups. A joint analysis of the morphological variables of D. maidis males and females showed a high canonical correlation with the geographic variables (latitude and elevation) of the localities where the specimens were collected. Positive and highly signiÞcant correlations of 0.97 (F ⫽ 16.4; P ⬍ 0.01; df ⫽ 10,38) and 0.98 (F ⫽ 15.5; P ⬍ 0.01; df ⫽ 12,36) were obtained for males and females, respectively, by applying the WilkÕs lambda test; similar results were obtained by using the other multivariate tests. A separate analysis of the association of each morphological variable with the latitude and elevation of the collecting localities yielded signiÞcant correlations for both females and males of D. maidis (Table 4). The correlations were positive for weight, interocular distance, length of left and right wings, and length of ovipositor, showing that D. maidis adults collected in the central-south region of the country (higher southern latitudes) or at higher elevations tend to be heavier and larger than those collected in northeastern Brazil (lower northern latitudes) or at lower elevations. A positive correlation was also observed between abdomen pigmentation

and the geographic variables (Table 4). There was a signiÞcant negative correlation between the mean annual temperature and the latitude (R2 ⫽ ⫺0.83; t ⫽ 7.33; P ⬍ 0.01) and elevation (R2 ⫽ ⫺0.76; t ⫽ 5.90; P ⬍ 0.01) of the collecting localities, indicating that higher latitudes and/or elevations are associated with lower temperatures. Except for wing length, the morphological variables evaluated in D. maidis adults seem to be more inßuenced by the latitude than by the elevation of the collecting localities, because the correlation values were higher for latitude (Table 4). Discussion This study shows morphological differences among populations of D. maidis from different regions in Brazil. The joint analysis of all morphological variables allowed the separation of two distinct groups, according to the collecting site: (1) populations from the northeast region and (2) populations from the centralsouth region. The morphological differences observed were associated with variations in latitude and elevation of the collecting sites. An increase in body weight, size, and pigmentation was observed in higher latitudes and elevations. For example, males and females from Castro/PR (24⬚47⬘28⬙ S; group 2) show, respectively, head capsules that are 18 and 12% wider and left wings that are 17 and 15% longer and are considerably heavier (72 and 44%, respectively) and darker than

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Table 3. Means ⴞ SEM of morphological variables related to body size, weight, and pigmentation of females of D. maidis collected in different Brazilian localities Region Northeast

Central-south

Collecting locality

Dry weight (mg)a

Interocular distance (mm)

Left wing (mm)b

Right wing (mm)b

Ovipositor (mm)c

Light intensity (␮E/s/m2)d

Ne

Ipanguaç u/RN Ceara´-Mirim/RN Lagoa Grande/PE Petrolina/PE Juazeiro/BA Barreiras/BA Brasõ´lia/DF Rio Verde/GO Itumbiara/GO Sete Lagoas/MG Divino´ polis/MG Guaõ´ra/SP Franca/SP Passos/MG Brodowski/SP Lavras/MG Cravinhos/SP Bonito/MS Poç os de Caldas/MG Piracicaba/SP Campos do Jordaõ/SP Jacarezinho/PR Arapongas/PR Toledo/PR Castro/PR Chapeco´ /SC

0.36 ⫾ 0.005 0.25 ⫾ 0.005 0.35 ⫾ 0.005 0.37 ⫾ 0.006 0.36 ⫾ 0.004 0.31 ⫾ 0.007 Ñ 0.42 ⫾ 0.010 0.39 ⫾ 0.003 0.39 ⫾ 0.006 0.45 ⫾ 0.002 0.34 ⫾ 0.007 0.49 ⫾ 0.003 0.43 ⫾ 0.002 0.54 ⫾ 0.006 0.49 ⫾ 0.007 0.41 ⫾ 0.003 0.34 ⫾ 0.005 0.50 ⫾ 0.008 0.41 ⫾ 0.008 0.52 ⫾ 0.006 0.40 ⫾ 0.012 0.47 ⫾ 0.002 0.51 ⫾ 0.003 0.52 ⫾ 0.009 0.56 ⫾ 0.003

0.43 ⫾ 0.005 0.41 ⫾ 0.020 0.44 ⫾ 0.006 0.44 ⫾ 0.004 0.44 ⫾ 0.006 0.45 ⫾ 0.005 Ñ 0.47 ⫾ 0.007 0.48 ⫾ 0.007 0.46 ⫾ 0.006 0.47 ⫾ 0.007 0.48 ⫾ 0.005 0.48 ⫾ 0.006 0.48 ⫾ 0.006 0.51 ⫾ 0.008 0.49 ⫾ 0.007 0.47 ⫾ 0.003 0.46 ⫾ 0.007 0.50 ⫾ 0.009 0.47 ⫾ 0.006 0.50 ⫾ 0.005 0.47 ⫾ 0.006 0.49 ⫾ 0.005 0.47 ⫾ 0.009 0.49 ⫾ 0.004 0.51 ⫾ 0.010

1.65 ⫾ 0.015 1.69 ⫾ 0.048 1.70 ⫾ 0.016 1.61 ⫾ 0.016 1.65 ⫾ 0.018 1.73 ⫾ 0.018 Ñ 1.79 ⫾ 0.022 1.78 ⫾ 0.024 1.77 ⫾ 0.015 1.81 ⫾ 0.029 1.73 ⫾ 0.024 1.85 ⫾ 0.020 1.84 ⫾ 0.012 1.85 ⫾ 0.032 1.84 ⫾ 0.016 1.76 ⫾ 0.024 1.80 ⫾ 0.031 1.85 ⫾ 0.028 1.74 ⫾ 0.016 1.85 ⫾ 0.016 1.75 ⫾ 0.025 1.81 ⫾ 0.017 1.80 ⫾ 0.018 1.89 ⫾ 0.019 1.84 ⫾ 0.033

1.62 ⫾ 0.019 1.62 ⫾ 0.035 1.65 ⫾ 0.020 1.61 ⫾ 0.011 1.65 ⫾ 0.019 1.70 ⫾ 0.017 Ñ 1.74 ⫾ 0.022 1.77 ⫾ 0.024 1.74 ⫾ 0.015 1.76 ⫾ 0.024 1.67 ⫾ 0.027 1.81 ⫾ 0.020 1.79 ⫾ 0.016 1.81 ⫾ 0.016 1.83 ⫾ 0.016 1.75 ⫾ 0.028 1.76 ⫾ 0.037 1.81 ⫾ 0.027 1.74 ⫾ 0.019 1.79 ⫾ 0.027 1.74 ⫾ 0.026 1.80 ⫾ 0.020 1.75 ⫾ 0.022 1.86 ⫾ 0.019 1.81 ⫾ 0.034

0.85 ⫾ 0.027 0.82 ⫾ 0.029 0.83 ⫾ 0.012 0.85 ⫾ 0.010 0.83 ⫾ 0.018 0.78 ⫾ 0.014 Ñ 0.88 ⫾ 0.020 0.83 ⫾ 0.014 0.87 ⫾ 0.013 0.93 ⫾ 0.008 0.94 ⫾ 0.011 0.93 ⫾ 0.011 0.95 ⫾ 0.023 0.90 ⫾ 0.023 0.92 ⫾ 0.015 0.84 ⫾ 0.023 0.86 ⫾ 0.020 0.92 ⫾ 0.012 0.84 ⫾ 0.015 0.97 ⫾ 0.014 0.85 ⫾ 0.015 0.91 ⫾ 0.013 0.93 ⫾ 0.022 0.96 ⫾ 0.014 1.03 ⫾ 0.043

1.55 ⫾ 0.075 1.30 ⫾ 0.133 1.16 ⫾ 0.110 1.37 ⫾ 0.100 1.35 ⫾ 0.097 0.96 ⫾ 0.083 Ñ 0.98 ⫾ 0.086 0.74 ⫾ 0.147 0.48 ⫾ 0.097 0.85 ⫾ 0.155 0.34 ⫾ 0.056 0.93 ⫾ 0.115 0.60 ⫾ 0.151 1.06 ⫾ 0.073 0.75 ⫾ 0.112 0.53 ⫾ 0.092 0.70 ⫾ 0.193 0.48 ⫾ 0.129 0.66 ⫾ 0.119 0.28 ⫾ 0.037 0.42 ⫾ 0.086 0.48 ⫾ 0.068 0.44 ⫾ 0.062 0.31 ⫾ 0.064 0.88 ⫾ 0.103

10 3 10 10 10 10 1 10 10 10 10 10 10 10 10 10 10 5 10 10 10 10 10 10 10 7

a

Dry body weight (without wings). Winglength, represented by the length of the second median cell of the forewing. Ovipositor length, measured from the seventh sternite up to the tip of the ovipositor. d Light intensity transmited through the slide picture of the abdomen (lower values indicate darker specimens). e Number of individuals analyzed. b c

those from Ipanguaç u/RN (05⬚29⬘54⬙ S; group 1; Tables 2 and 3). Morphological variations of insects along gradients of latitude and elevation are well studied (Cushman et al. 1993, Hawkins and Lawton 1995, Krasnov et al. 1996, Smith et al. 2000). In the case of D. maidis in Brazil, latitude seems to be the major factor inßuencing the separation of groups 1 and 2, with localities of these two groups from two distinct ranges of latitudes. However, the role of elevation cannot be ruled out, because the localities of group 1 are lower in elevation (⬍500 m) than most localities of group 2 (Table 1).

Temperature and humidity are major factors controlling polymorphism in insects, particularly in regions close to the equator (Tauber et al. 1986). Temperature seems to be an important factor inducing the polymorphism in D. maidis, because it is highly correlated with the latitude and elevation of the collecting localities. Mean annual temperatures of localities from group 1 (northeast) are higher than those from group 2 (center and south; Table 1). It is interesting to point out that even the leafhopper samples from Ipanguaç u/RN, Petrolina/PE, and Juazeiro/BA (group 1), which were collected in the winter (Au-

Fig. 2. Dendogram based on all morphological variables of D. maidis females built by the method of unweighted pair-group method with arithmetic average (“unweighted pair group method of arithmetic means”; see Table 1 for abbreviations).

Fig. 3. Dendogram based on all morphological variables of D. maidis males built by the method of unweighted pairgroup method with arithmetic average (“unweighted pair group method of arithmetic means”; see Table 1 for abbreviations).

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Table 4. Pearson’s correlation between morphological variables of D. maidis adults and geographic variables (latitude and elevation) of the collecting localities Gender Females

Geographic variable Latitude Elevation

Males

Latitude Elevation

Body wta f

0.75 0.0001g 0.69 0.0001g 0.86f 0.0001g 0.77 0.0001g

Interocular distanceb

Left wingc

Right wingc

Ovipositord

Light intensitye

0.85 0.0001g 0.73 0.0001g 0.87 0.0001g 0.54 0.0050g

0.73 0.0001g 0.81 0.0001g 0.77 0.0001g 0.78 0.0001g

0.78 0.0001g 0.79 0.0001g 0.78 0.0001g 0.69 0.0001g

0.70 0.0001g 0.54 0.0050g Ñ Ñ Ñ Ñ

⫺0.82 0.0001g ⫺0.53 0.0060g ⫺0.78 0.0001g ⫺0.69 0.0001g

a

Dry body weight without wings. Indicative of head capsule width. Winglength, represented by the length of the second medium cell of the forewing. d Ovipositor length, measured from the seventh sternite up to the tip of the ovipositor. e Light intensity transmited through the slide picture of the abdomen (lower values indicate darker specimens). f Correlation coefÞcient (gsigniÞcant correlation by t-test: P ⬍ 0.01). b c

gust), showed lower body weight and size and lighter pigmentation than those from localities of group 2, which were sampled mostly in the summer and fall (DecemberÐMay). This probably occurred because average temperatures in the northeast region (which is close to the equator) are relatively high (ⱖ25⬚C) during the winter. Average winter temperatures in the northeast are similar or slightly higher than those of summer in the central-south region (http://www. climabrasileiro.hpg.ig.com.br). In Mexico (Jalisco), where winter temperatures are lower, Larsen and Nault (1994) observed that male and female adults of D. maidis collected during the dry winter season in October and March were darker and larger than those collected in May (spring). In this study, no clear differences were observed in adult size and pigmentation between males and females collected during the summer (January) in Ipanguaç u/RN, Petrolina/PE, and Juazeiro/BA and those collected during the winter (August) in Ceara´-Mirim/RN and Lagoa Grande/PE, which are all localities within the same range of latitude and elevations (⬍400 m) in the northeast region (Tables 1Ð3). The inßuence of environmental factors such as temperature and photoperiod on the nymphal stage of leafhoppers is reßected in variations of resulting adults (Harrison 1980). Larsen and Nault (1994) observed an increased size, weight, and pigmentation in adult Dalbulus when insects were reared at lower temperatures and shorter days. For Eupteryx urticae (Fabr.), there is a positive correlation between darker forms and higher elevations, suggesting that temperature, inßuenced by elevation, could be the most important factor in development of these forms (Stewart 1981). Latitude and temperature are strongly correlated variables, although in some cases, temperature can be markedly inßuenced by elevation as well. BergmannÕs rule predicts that animal body size tends to increase with the increment of latitude (Bergmann 1847). Our results indicate that D. maidis populations from Brazil follow BergmannÕs rule, showing a tendency of increase in the evaluated morphologic variables (weight and size) at higher latitudes (Tables 2Ð 4). The Þrst

explanation for BergmannÕs rule, as a mechanism for heat conservation, has been rejected (Scholander 1955, Cushman et al. 1993, Blackburn et al. 1999). Other adaptive and nonadaptive explanations have been suggested, such as hypotheses concerning phylogenetic history, migration ability, and resistance against starvation (Cushman et al. 1993, Blackburn et al. 1999). Morphological changes in insects are often adaptive strategies to the conditions to which they are exposed. For D. maidis, the appearance of darker forms in the central-south region may be associated with thermal regulation. Darker forms absorb more solar energy to heat their bodies (Fields and McNeil 1988, Larsen et al. 1993), which may be important in colder localities in Brazil, such as Campos do Jordaõ/ SP, Castro/PR, and Chapeco´ /SC, with mean annual temperatures of 14.8, 16.2, and 18.7⬚C, respectively. The increase in body weight and size is probably caused by slower development rates under lower temperatures and longer photophase, which allows longer feeding and growth periods (Larsen and Nault 1994) and accumulation of higher amounts of reserves to go through long periods without nourishment. Regardless of the collecting site, D. maidis females are always larger and heavier than males. Gender differences have been previously reported for leafhoppers. Males and females of D. maidis, D. elimatus (Ball), D. gelbus DeLong, D. quiquenotatus DeLong and Nault, and Baldulus tripsaci Kramer and Whitcomb reared under laboratory conditions show signiÞcant variations in size and weight (Larsen and Nault 1994). Regarding body pigmentation, differences in rearing condition affected pigmentation of D. maidis, D. elimatus, and D. gelbus, but not of D. quiquenotatus and B. tripsaci (Larsen and Nault 1994). For the black-faced leafhopper, G. nigrifrons, reared under Þve different temperatures, females were always bigger and heavier than males (Larsen et al. 1990). The differences in weight and size between sexes of D. maidis may be related to the development rate: females develop more slowly than males; thus, they have more time to feed and grow (Larsen and Nault 1994). From an adaptive standpoint, bigger and heavier fe-

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males are more likely to nurture and carry more eggs than small females (Larsen and Nault 1994). The fore wing asymmetry of D. maidis veriÞed in this study relates to the longer left wing covering the right one when the leafhopper is resting. The results of this survey indicate that D. maidis is possibly the only species of the genus Dalbulus occurring on maize in Brazil. These results are in accordance with those reported by Oman (1948), Triplehorn and Nault (1985), and Madden et al. (1986), who considered the corn leafhopper as the most widespread Dalbulus species, occurring from the southern United States to Argentina, a result of its high mobility and close association with cultivated maize (Ga´mez 1983). D. maidis was Þrst reported in Brazil by Mendes (1938). Interestingly, we also collected some adults of D. maidis on S. bicolor in Sete Lagoas/MG, conÞrming a previous report that the corn leafhopper can be found on cultivated sorghum (Waquil 1997). There was no evidence that D. maidis used S. bicolor as a developmental host. It is possible that the polymorphism observed among populations of D. maidis from the northeast (group 1) and central-south (group 2) regions of Brazil has a genetic basis. These populations are separated by a considerable geographical distance, and consequently, are subject to different selection pressures. The northeast and central-south regions are distinct with respect to environmental conditions, particularly climate (e.g., temperature, relative humidity, and rainfall) and vegetation. Genetic differences are expected when the gene ßow among the populations is low and selection pressure is variable, which can occur among geographically distant populations along a latitude gradient (Mosseau and Roff 1995). Currently we are evaluating the morphological differences for D. maidis to determine whether such differences have a genetic basis rather than or in addition to the expected inßuence of environmental factors such as temperature. Acknowledgments The authors thank A. M. Auad, E. L. Arau´ jo, L. Presotti, J. M. Waquil, D. N. Ferreira, E. Oliveira, G. S. Belchior, M.A.U. Fernandes, R. Fustioni, P. Tironi, J. M. Milanez, A. D. Gru¨ ztmacher, and J. J. Carbonari for shipping leafhopper samples from distant locations, as well as the Brazilian funding agencies, CNPq and CAPES, for providing scholarships to the Þrst author.

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Stewart, A.J.A. 1981. Nynphal polymorphism in two species of Eupteryx (Curt.) Acta Entomol. Fenn. 38: 43. Tauber, J. M., A. C. Tauber, and S. Masaki. 1986. Insect adaptation to environmental change, pp. 7Ð37. In J. M. Tauber, A. C. Tauber, and S. Masaki (eds.), Seasonal adaptations of insects. Oxford University Press, New York. Triplehorn, B. W., and L. R. Nault. 1985. Phylogenetic classiÞcation of the genus Dalbulus (Homoptera: Cicadelli-

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