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,1JOA˜O ROBERTO SPOTTI LOPES,2 CARLOS TADEU DOS SANTOS DIAS,2ANDLOWELL R. NAULT3
Departamento de Entomologia, Fitopatologia e Zoologia Agrõ´cola, Escola Superior de Agricultura “Luizde Queiroz,” Universidade de Sa˜o 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. maidiswas the only Dalbulus species found in the samples. Up to 10 males and 10 females of D. maidisfrom 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 Variac¸o˜es morfolo´gicas em insetos podem ser inßuenciadas por latitude e elevac¸a˜o. Neste
estudo no´s mostraˆmos que esses dois paraˆmetros inßuenciam marcadamente a apareˆncia da cigarrinha-do-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 elevac¸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 feˆmeas de D. maidisde cada local de coleta, quanto ao tamanho, pigmentac¸a˜o e peso do corpo. Feˆmeas foram sempre maiores e mais pesadas que os machos em uma mesma localidade. Para ambos os sexos, houve uma correlac¸a˜o positiva e signiÞcativa entre as varia´veis morfolo´gicas avaliadas e a latitude e elevac¸a˜o de onde os espe´cimes foram coletados. Espe´cimes coletados em latitudes mais altas (regia˜o Centro-Sul) foram maiores, mais pigmentados e pesados do que aqueles de menores latitudes (regia˜o Nordeste). Houve tambe´m uma tendeˆncia de aumento do peso do corpo, largura da capsula cefa´lica e comprimento da asa em maiores elevac¸o˜es.
KEY WORDS insect vector, morphological variation, Zea mays
THE DELTOCEPHALINE LEAFHOPPER GENUSDalbulus
De-Long includes 13 species distributed in the American continent, primarily in Mexico and Guatemala. Leaf-hopper 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
Nault 1985). This leafhopper is the vector of three pathogens associated with corn stunt disease, the maize rayado Þno maraÞvirus (MRFV), and the mol-licutes, Spiroplasma kunkelii Whitcomb (“corn stunt spiroplasma” [CSS]) and maize bushy stunt phyto-plasma (MBSP), which are limiting factors to maize production in Latin America (Nault 1990, Oliveira et al. 1998).
Dalbulus maidisoccurs throughout the neotropics, from the southern United States to northern Argentina (Oman 1948, Triplehorn and Nault 1985). It is the only Dalbulusspecies recorded on maize in South America. Because the corn leafhopper has such a wide distri-bution, it would be expected that morphological and physiological variations occur among its populations.
1Corresponding author: Embrapa Cerrados, C. Postal 08223,
Plan-altina DF 73310-970, Brazil. E-mail: charles@cpac.embrapa.br.
2Escola Superior de Agricultura “Luizde Queiroz,” Universidade
de Sa˜o Paulo, C. Postal 9, Piracicaba SP 13418-900, Brazil.
3Department of Entomology, Ohio Agricultural Research and
De-velopment Center, The Ohio State University, Wooster, OH 44691. 0046-225X/04/1192Ð1199$04.00/0 䉷 2004 Entomological Society of America
These variations likely would help the corn leafhopper cope with varying environmental conditions that oc-cur 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 de-clines.
Many insect species vary in size and coloration in response to environmental conditions. This polymor-phism aids in dormancy, thermoregulation, reproduc-tion, 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 en-vironmental 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 Gra-minella nigrifrons(Forbes) (Larsen et al. 1990). Poly-morphism has also been observed along latitudinal and elevational gradients for several insect groups (Cush-man 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 popula-tions along a range of latitudes and elevapopula-tions 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 (Decem-berÐJune), except for those in Guaõ´ra/SP and Bonito/ MS, which were carried out in the spring, and Ipan-guac¸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, leaf-hoppers were also collected from sorghum (Sorghum bicolorL. Moench), Brachiaria sp., and B. plantaginea (Link). Species identiÞcation was performed as de-scribed 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 mea-sured for the distance between the compound eyes in the head vertex, the length of the second medium cell Table 1. Brazilian localities where leafhoppers were sampled on maize
Region Locality Abbreviation Collecting date Latitude (S) Elevation (m) Temperature (⬚C)a Nb
Northeast Ipanguac¸u/RN Ip 8/19/1996 05⬚29⬘54⬙ 16 27.2 180 Ceara´-Mirim/RN CM 1/17/1996 05⬚38⬘04⬙ 33 25.4 8 Lagoa Grande/PE LG 1/19/1996 08⬚59⬘49⬙ 300 26.4 470 Petrolina/PE Pe 8/23/1996 09⬚23⬘55⬙ 376 26.3 207 Juazeiro/BA Ju 8/22/1996 09⬚24⬘42⬙ 368 26.3 157 Barreiras/BA Ba 5/9/1995 12⬚09⬘10⬙ 452 24.3 85 Central-south Brasõ´lia/DF Br 1/10/1996 15⬚46⬘47⬙ 1,171 21.2 4 Rio Verde/GO RV 7/8/1995 17⬚47⬘53⬙ 715 22.5 205 Itumbiara/GO It 5/29/1996 18⬚25⬘09⬙ 448 19.0 108 Sete Lagoas/MG SL 5/19/1995 19⬚27⬘57⬙ 761 20.9 333 Divino´polis/MG Di 1/5/1996 20⬚08⬘20⬙ 712 23.0 127 Guaõ´ra/SP Gu 11/6/1995 20⬚19⬘06⬙ 517 23.6 463 Anasta´cio/MS Na 1/4/1996 20⬚29⬘01⬙ 160 21.0 5 Franca/SP Fr 2/26/1996 20⬚32⬘19⬙ 996 20.1 174 Passos/MG Pa 3/23/1996 20⬚43⬘08⬙ 745 20.7 90 Brodowski/SP Bd 2/27/1996 20⬚59⬘29⬙ 861 20.8 117 Bonito/MS Bo 10/2/1995 21⬚07⬘16⬙ 315 22.0 5 Lavras/MG La 1/9/1996 21⬚14⬘43⬙ 919 19.4 55 Cravinhos/SP Cr 5/12/1995 21⬚20⬘25⬙ 788 21.0 128 Poc¸os de Caldas/MG PC 4/8/1996 21⬚47⬘16⬙ 1,196 17.0 134 Piracicaba/SP Pi 3/6/1996 22⬚43⬘31⬙ 547 21.6 517 Campos do Jorda˜o/SP CJ 4/3/1996 22⬚44⬘22⬙ 1,628 14.8 88 Jacarezinho/PR Ja 5/4/1996 23⬚09⬘38⬙ 501 20.3 131 Arapongas/PR Ar 3/27/1996 23⬚25⬘10⬙ 729 21.0 317 Toledo/PR To 3/12/1996 24⬚42⬘49⬙ 560 19.8 257 Castro/PR Ca 3/13/1996 24⬚47⬘28⬙ 999 16.2 285 Chapeco´/SC Ch 12/18/1995 27⬚05⬘47⬙ 674 18.7 11
aMean annual temperature (Departamento Nacional de Metereologia 1992). bNumber of individuals sampled in each locality.
of the fore wings (Larsen et al. 1990), and the length of the ovipositor, from the hollow portion of the sev-enth sternite to its tip.
The intensity of abdomenal pigmentation was eval-uated as an indicator of body coloration. Leafhooper wings were removed to expose the back of the abdo-men from the third to the Þfth segabdo-ment. Groups of Þve individuals, separated according to sex, were placed onto a microscopic slide with a small amount of glyc-erin to keep them in the dorsal position and photo-graphed with a slide Þlm (Fuji RDP II ASA 100, Fuji Photo Film da Amazoˆnia 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 Amazoˆnia 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 in-tensity (E/s/m) transmitted through the abdomen image. A photometer (model LI-189, LI-COR, Lin-coln, NE, USA) equipped with a Quantum-type sensor (LI-190SA; LI-COR, Lincoln, NE) was used to mea-sure light intensity. The darker the abdomen exoskel-eton, 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⫺5g precision electric scale.
Statistical Analysis. The data on leafhopper size
(in-terocular distance, wing, and ovipositor length), pig-mentation, and dry weight were analyzed by the Sta-tistical Analysis System V. 6.08 (SAS Institute 1993). For sex comparison, a univariate analysis of variance (ANOVA) of the morphological variables was per-formed 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-Law-leyÕs Trace, and RoyÕs Greatest Root (SAS Institute
1993). Separately for each sex, a PearsonÕs correlation analysis was performed between each of the morpho-logical variables and the latitude and elevation of the collecting sites, as well as a correlation between the latitude and elevation and the mean annual temper-atures of each of the localities. In addition, a canonical correlation analysis (SAS Institute 1993) was per-formed between the set of morphological and geo-graphic variables (latitude and elevation). The canon-ical 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 un-weighted pair group method of arithmetic means (un-weighted pair-group method with arithmetic average; SAS Institute 1993) was performed by combining all set of morphological variables.
Dalbulus maidisvoucher specimens were deposited with the Entomology Museum of the Escola Superior de Agricultura “Luizde Queiroz”/USP, Brazil.
Results
Dalbulus maidiswas the only species of the genus Dalbulusfound 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 sor-ghum in Sete Lagoas/MG, but less frequently (around 15%) than leafhopper species of other genera. In sam-ples collected in Brachiaria sp. and Brachiaria plan-taginea(Link), also from Sete Lagoas/MG, no Dalbu-lusleafhoppers 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 inter-ocular 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 differ-ence 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 mul-tidimensional 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 morpholog-ical 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 in-cludes localities between the latitudes 05⬚29⬘54⬙ and
Fig. 1. Map showing the collection localities of D. maidis in Brazil. (see Table 1 for abbreviations).
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 sep-aration of the two groups (Table 1). Several subgroups are observed within group 2 for both genders. Differ-ences in latitude or elevation do not seem to explain the separation of these subgroups.
A joint analysis of the morphological variables of D. maidismales 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 corre-lations 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. maidisadults 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 lat-itudes) 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 an-nual 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 inßu-enced 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, accord-ing to the collectaccord-ing site: (1) populations from the northeast region and (2) populations from the central-south region. The morphological differences observed were associated with variations in latitude and eleva-tion of the collecting sites. An increase in body weight, size, and pigmentation was observed in higher lati-tudes and elevations. For example, males and females from Castro/PR (24⬚47⬘28⬙ S; group 2) show, respec-tively, 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 Table 2. Meansⴞ SEM of morphological variables related to body size, weight, and pigmentation of males of D. maidis collected in different Brazilian localities
Region Collecting locality Dry weight(mg)a
Interocular distance
(mm)
Left wing
(mm)b Right wing(mm)b Light intensity(E/s/m2)c Nd
Northeast Ipanguac¸u/RN 0.18 ⫾ 0.010 0.39 ⫾ 0.005 1.51 ⫾ 0.018 1.51 ⫾ 0.019 1.56 ⫾ 0.068 10 Ceara´-Mirim/RN 0.15 ⫾ 0.004 0.37 ⫾ 0.008 1.52 ⫾ 0.018 1.51 ⫾ 0.017 1.19 ⫾ 0.073 5 Lagoa Grande/PE 0.17 ⫾ 0.009 0.40 ⫾ 0.005 1.54 ⫾ 0.067 1.52 ⫾ 0.017 1.15 ⫾ 0.135 10 Petrolina/PE 0.19 ⫾ 0.006 0.39 ⫾ 0.004 1.54 ⫾ 0.021 1.50 ⫾ 0.020 1.44 ⫾ 0.127 10 Juazeiro/BA 0.18 ⫾ 0.004 0.41 ⫾ 0.006 1.55 ⫾ 0.014 1.50 ⫾ 0.015 1.32 ⫾ 0.093 10 Barreiras/BA 0.22 ⫾ 0.003 0.41 ⫾ 0.042 1.53 ⫾ 0.013 1.55 ⫾ 0.018 1.22 ⫾ 0.122 10 Central-south Brasõ´lia/DF 0.23 ⫾ 0.009 0.43 ⫾ 0.003 1.70 ⫾ 0.015 1.69 ⫾ 0.014 0.44 ⫾ 0.260 3 Rio Verde/GO 0.25 ⫾ 0.010 0.44 ⫾ 0.005 1.70 ⫾ 0.014 1.66 ⫾ 0.013 0.88 ⫾ 0.155 10 Itumbiara/GO 0.23 ⫾ 0.008 0.42 ⫾ 0.005 1.63 ⫾ 0.028 1.60 ⫾ 0.021 0.74 ⫾ 0.136 10 Sete Lagoas/MG 0.26 ⫾ 0.004 0.44 ⫾ 0.007 1.67 ⫾ 0.017 1.65 ⫾ 0.011 0.39 ⫾ 0.070 10 Divino´polis/MG 0.24 ⫾ 0.008 0.45 ⫾ 0.004 1.63 ⫾ 0.024 1.60 ⫾ 0.021 0.73 ⫾ 0.121 10 Guaõ´ra/SP 0.24 ⫾ 0.007 0.44 ⫾ 0.007 1.65 ⫾ 0.014 1.63 ⫾ 0.014 0.30 ⫾ 0.032 10 Franca/SP 0.29 ⫾ 0.012 0.44 ⫾ 0.004 1.69 ⫾ 0.028 1.65 ⫾ 0.028 0.44 ⫾ 0.067 10 Anasta´cio/MS 0.19 ⫾ 0.007 0.45 ⫾ 0.012 1.63 ⫾ 0.046 1.58 ⫾ 0.070 0.88 ⫾ 0.137 5 Passos/MG 0.28 ⫾ 0.005 0.43 ⫾ 0.004 1.72 ⫾ 0.013 1.68 ⫾ 0.017 0.60 ⫾ 0.109 10 Brodowski/SP 0.29 ⫾ 0.006 0.44 ⫾ 0.011 1.71 ⫾ 0.032 1.67 ⫾ 0.031 0.78 ⫾ 0.126 10 Lavras/MG 0.29 ⫾ 0.008 0.45 ⫾ 0.004 1.75 ⫾ 0.015 1.70 ⫾ 0.019 0.53 ⫾ 0.127 10 Cravinhos/SP 0.22 ⫾ 0.003 0.43 ⫾ 0.030 1.65 ⫾ 0.011 1.62 ⫾ 0.020 0.29 ⫾ 0.049 10 Poc¸os de Caldas/MG 0.29 ⫾ 0.007 0.44 ⫾ 0.004 1.75 ⫾ 0.026 1.69 ⫾ 0.034 0.25 ⫾ 0.072 10 Piracicaba/SP 0.23 ⫾ 0.005 0.43 ⫾ 0.004 1.63 ⫾ 0.024 1.58 ⫾ 0.020 0.49 ⫾ 0.666 10 Campos do Jorda˜o/SP 0.32 ⫾ 0.002 0.45 ⫾ 0.004 1.70 ⫾ 0.014 1.67 ⫾ 0.015 0.18 ⫾ 0.024 10 Jacarezinho/PR 0.24 ⫾ 0.007 0.43 ⫾ 0.006 1.64 ⫾ 0.016 1.63 ⫾ 0.017 0.36 ⫾ 0.086 10 Arapongas/PR 0.26 ⫾ 0.003 0.43 ⫾ 0.009 1.67 ⫾ 0.027 1.65 ⫾ 0.013 0.39 ⫾ 0.067 10 Toledo/PR 0.28 ⫾ 0.003 0.44 ⫾ 0.004 1.70 ⫾ 0.026 1.66 ⫾ 0.014 0.30 ⫾ 0.054 10 Castro/PR 0.31 ⫾ 0.002 0.46 ⫾ 0.007 1.76 ⫾ 0.022 1.73 ⫾ 0.016 0.14 ⫾ 0.023 10 Chapeco´/SC 0.30 ⫾ 0.006 0.50 ⫾ 0.024 1.72 ⫾ 0.036 1.70 ⫾ 0.036 0.83 ⫾ 0.169 4
aDry body weight (without wings).
bWinglength, represented by the length of the second median cell of the forewing.
cLight intensity transmited through the slide picture of the abdomen (lower values indicate darker specimens). dNumber of individuals analyzed.
those from Ipanguac¸u/RN (05⬚29⬘54⬙ S; group 1; Ta-bles 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. How-ever, 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 con-trolling polymorphism in insects, particularly in re-gions close to the equator (Tauber et al. 1986). Tem-perature seems to be an important factor inducing the polymorphism in D. maidis, because it is highly cor-related with the latitude and elevation of the collect-ing 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 Ipanguac¸u/RN, Petrolina/PE, and Juazeiro/BA (group 1), which were collected in the winter (Au-Table 3. Meansⴞ SEM of morphological variables related to body size, weight, and pigmentation of females of D. maidis collected in different Brazilian localities
Region 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 Northeast Ipanguac¸u/RN 0.36 ⫾ 0.005 0.43 ⫾ 0.005 1.65 ⫾ 0.015 1.62 ⫾ 0.019 0.85 ⫾ 0.027 1.55 ⫾ 0.075 10 Ceara´-Mirim/RN 0.25 ⫾ 0.005 0.41 ⫾ 0.020 1.69 ⫾ 0.048 1.62 ⫾ 0.035 0.82 ⫾ 0.029 1.30 ⫾ 0.133 3 Lagoa Grande/PE 0.35 ⫾ 0.005 0.44 ⫾ 0.006 1.70 ⫾ 0.016 1.65 ⫾ 0.020 0.83 ⫾ 0.012 1.16 ⫾ 0.110 10 Petrolina/PE 0.37 ⫾ 0.006 0.44 ⫾ 0.004 1.61 ⫾ 0.016 1.61 ⫾ 0.011 0.85 ⫾ 0.010 1.37 ⫾ 0.100 10 Juazeiro/BA 0.36 ⫾ 0.004 0.44 ⫾ 0.006 1.65 ⫾ 0.018 1.65 ⫾ 0.019 0.83 ⫾ 0.018 1.35 ⫾ 0.097 10 Barreiras/BA 0.31 ⫾ 0.007 0.45 ⫾ 0.005 1.73 ⫾ 0.018 1.70 ⫾ 0.017 0.78 ⫾ 0.014 0.96 ⫾ 0.083 10 Central-south Brasõ´lia/DF Ñ Ñ Ñ Ñ Ñ Ñ 1 Rio Verde/GO 0.42 ⫾ 0.010 0.47 ⫾ 0.007 1.79 ⫾ 0.022 1.74 ⫾ 0.022 0.88 ⫾ 0.020 0.98 ⫾ 0.086 10 Itumbiara/GO 0.39 ⫾ 0.003 0.48 ⫾ 0.007 1.78 ⫾ 0.024 1.77 ⫾ 0.024 0.83 ⫾ 0.014 0.74 ⫾ 0.147 10 Sete Lagoas/MG 0.39 ⫾ 0.006 0.46 ⫾ 0.006 1.77 ⫾ 0.015 1.74 ⫾ 0.015 0.87 ⫾ 0.013 0.48 ⫾ 0.097 10 Divino´polis/MG 0.45 ⫾ 0.002 0.47 ⫾ 0.007 1.81 ⫾ 0.029 1.76 ⫾ 0.024 0.93 ⫾ 0.008 0.85 ⫾ 0.155 10 Guaõ´ra/SP 0.34 ⫾ 0.007 0.48 ⫾ 0.005 1.73 ⫾ 0.024 1.67 ⫾ 0.027 0.94 ⫾ 0.011 0.34 ⫾ 0.056 10 Franca/SP 0.49 ⫾ 0.003 0.48 ⫾ 0.006 1.85 ⫾ 0.020 1.81 ⫾ 0.020 0.93 ⫾ 0.011 0.93 ⫾ 0.115 10 Passos/MG 0.43 ⫾ 0.002 0.48 ⫾ 0.006 1.84 ⫾ 0.012 1.79 ⫾ 0.016 0.95 ⫾ 0.023 0.60 ⫾ 0.151 10 Brodowski/SP 0.54 ⫾ 0.006 0.51 ⫾ 0.008 1.85 ⫾ 0.032 1.81 ⫾ 0.016 0.90 ⫾ 0.023 1.06 ⫾ 0.073 10 Lavras/MG 0.49 ⫾ 0.007 0.49 ⫾ 0.007 1.84 ⫾ 0.016 1.83 ⫾ 0.016 0.92 ⫾ 0.015 0.75 ⫾ 0.112 10 Cravinhos/SP 0.41 ⫾ 0.003 0.47 ⫾ 0.003 1.76 ⫾ 0.024 1.75 ⫾ 0.028 0.84 ⫾ 0.023 0.53 ⫾ 0.092 10 Bonito/MS 0.34 ⫾ 0.005 0.46 ⫾ 0.007 1.80 ⫾ 0.031 1.76 ⫾ 0.037 0.86 ⫾ 0.020 0.70 ⫾ 0.193 5 Poc¸os de Caldas/MG 0.50 ⫾ 0.008 0.50 ⫾ 0.009 1.85 ⫾ 0.028 1.81 ⫾ 0.027 0.92 ⫾ 0.012 0.48 ⫾ 0.129 10 Piracicaba/SP 0.41 ⫾ 0.008 0.47 ⫾ 0.006 1.74 ⫾ 0.016 1.74 ⫾ 0.019 0.84 ⫾ 0.015 0.66 ⫾ 0.119 10 Campos do Jorda˜o/SP 0.52 ⫾ 0.006 0.50 ⫾ 0.005 1.85 ⫾ 0.016 1.79 ⫾ 0.027 0.97 ⫾ 0.014 0.28 ⫾ 0.037 10 Jacarezinho/PR 0.40 ⫾ 0.012 0.47 ⫾ 0.006 1.75 ⫾ 0.025 1.74 ⫾ 0.026 0.85 ⫾ 0.015 0.42 ⫾ 0.086 10 Arapongas/PR 0.47 ⫾ 0.002 0.49 ⫾ 0.005 1.81 ⫾ 0.017 1.80 ⫾ 0.020 0.91 ⫾ 0.013 0.48 ⫾ 0.068 10 Toledo/PR 0.51 ⫾ 0.003 0.47 ⫾ 0.009 1.80 ⫾ 0.018 1.75 ⫾ 0.022 0.93 ⫾ 0.022 0.44 ⫾ 0.062 10 Castro/PR 0.52 ⫾ 0.009 0.49 ⫾ 0.004 1.89 ⫾ 0.019 1.86 ⫾ 0.019 0.96 ⫾ 0.014 0.31 ⫾ 0.064 10 Chapeco´/SC 0.56 ⫾ 0.003 0.51 ⫾ 0.010 1.84 ⫾ 0.033 1.81 ⫾ 0.034 1.03 ⫾ 0.043 0.88 ⫾ 0.103 7 aDry body weight (without wings).
bWinglength, represented by the length of the second median cell of the forewing. cOvipositor length, measured from the seventh sternite up to the tip of the ovipositor.
dLight intensity transmited through the slide picture of the abdomen (lower values indicate darker specimens). eNumber of individuals analyzed.
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 pair-group method with arithmetic average (“unweighted pair group method of arithmetic means”; see Table 1 for abbre-viations).
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. maidiscollected during the dry winter season in October and March were darker and larger than those collected in May (spring). In this study, no clear dif-ferences were observed in adult size and pigmentation between males and females collected during the sum-mer (January) in Ipanguac¸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 lati-tude and elevations (⬍400 m) in the northeast region (Tables 1Ð3).
The inßuence of environmental factors such as tem-perature 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 Dal-buluswhen 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, inßu-enced 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 in-crease in the evaluated morphologic variables (weight and size) at higher latitudes (Tables 2Ð4). 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 phy-logenetic 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 Jorda˜o/ 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 tem-peratures 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 leaf-hoppers. Males and females of D. maidis, D. elimatus (Ball), D. gelbus DeLong, D. quiquenotatus DeLong and Nault, and Baldulus tripsaci Kramer and Whit-comb reared under laboratory conditions show sig-niÞcant variations in size and weight (Larsen and Nault 1994). Regarding body pigmentation, differ-ences in rearing condition affected pigmentation of D. maidis, D. elimatus,and D. gelbus, but not of D. quique-notatusand B. tripsaci (Larsen and Nault 1994). For the black-faced leafhopper, G. nigrifrons, reared under Þve different temperatures, females were always big-ger and heavier than males (Larsen et al. 1990). The differences in weight and size between sexes of D. maidismay be related to the development rate: fe-males develop more slowly than fe-males; thus, they have more time to feed and grow (Larsen and Nault 1994). From an adaptive standpoint, bigger and heavier fe-Table 4. Pearson’s correlation between morphological variables of D. maidis adults and geographic variables (latitude and elevation) of the collecting localities
Gender Geographic variable Body wta Interocular distanceb Left wingc Right wingc Ovipositord Light intensitye
Females Latitude 0.75f 0.85 0.73 0.78 0.70 ⫺0.82 0.0001g 0.0001g 0.0001g 0.0001g 0.0001g 0.0001g Elevation 0.69 0.73 0.81 0.79 0.54 ⫺0.53 0.0001g 0.0001g 0.0001g 0.0001g 0.0050g 0.0060g Males Latitude 0.86f 0.87 0.77 0.78 Ñ ⫺0.78 0.0001g 0.0001g 0.0001g 0.0001g Ñ 0.0001g Elevation 0.77 0.54 0.78 0.69 Ñ ⫺0.69 0.0001g 0.0050g 0.0001g 0.0001g Ñ 0.0001g
aDry body weight without wings. bIndicative of head capsule width.
cWinglength, represented by the length of the second medium cell of the forewing. dOvipositor length, measured from the seventh sternite up to the tip of the ovipositor.
eLight intensity transmited through the slide picture of the abdomen (lower values indicate darker specimens). fCorrelation coefÞcient (gsigniÞcant correlation by t-test: P ⬍ 0.01).
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 oc-curring on maize in Brazil. These results are in accor-dance with those reported by Oman (1948), Triple-horn and Nault (1985), and Madden et al. (1986), who considered the corn leafhopper as the most wide-spread 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. maidison 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 Bra-zil has a genetic basis. These populations are separated by a considerable geographical distance, and conse-quently, 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 rain-fall) 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 inßu-ence 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 fund-ing agencies, CNPq and CAPES, for providfund-ing scholarships to the Þrst author.
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