Influence of Altitude, Latitude and Season of Collection (Bergmann's Rule) on the Dimensions of Lutzomyia intermedia (Lutz & Neiva, 1912) (Diptera, Psychodidae, Phlebotominae)

Vol. 94(5): 693-700

Carlos Brisola Marcondes/⁺, Ana Leuch Lozovei*, Aloisio Falqueto**, Reginaldo P Brazil***, EAB Galati****, GM Aguiar*****, NA Souza*****

Departamento de Microbiologia e Parasitologia, Centro de Ciências Biológicas, Universidade Federal de Santa Catarina, Campus Trindade, 88040-900 Florianópolis, SC, Brasil *Departamento de Patologia Básica, SCB, UFPR, Curitiba, PR, Brasil **Centro Biomédico, UFES, Vitória, ES, Brasil ***Centro de Pesquisas René Rachou, Fiocruz, Belo Horizonte, MG, Brasil ****Faculdade de Saúde Pública, USP, São Paulo, SP, Brasil *****Departamento de Entomologia, Instituto Oswaldo Cruz, Rio de Janeiro, RJ, Brasil

The influence of altitude and latitude on some structure sizes of Lutzomyia intermedia was noted; several structures of insects collected in higher localities were greater, according to Bergmann's rule. This influence was more remarkable in two localities of the State of Espírito Santo, probably due to greater differences in altitude. Comparing insects from different latitudes, more differences were noted in comparisons of insects from low altitude localities than in those of material from higher altitudes. The small number of differences between insects collected in July and in December does not indicate a defined influence of season and temperature on the size of adults. The possible epidemiological implications of these variations are discussed.

Key words: altitude - latitude - Phlebotominae - Lutzomyia intermedia - Bergmann's Rule

The relationship between size and temperature was initially observed for endothermic animals and extended to insects, constituting Bergmann's rule (James 1970, Atkinson 1994). The altitude and latitude, in which the insects develop, through the temperature, can influence their size.

Lane (1988) cited preliminary studies on the influence of temperature upon the size of Lutzomyia longipalpis (Lutz & Neiva, 1912). This may be related to their fertility (Honek 1993) and epidemiological role (Haramis 1983, Kelly & Edman 1992). Lu. intermedia (Lutz & Neiva, 1912), redescribed by Marcondes (1996), has been incriminated as a vector of parasites causing cutaneous leishmaniasis (Rangel et al. 1984, Barros et al. 1985, Pereira & Hoch 1990, Aguiar 1993). Leishmania chagasi Cunha & Chagas, 1937 (Paraense & Chagas, 1940) and L. braziliensis Vianna, 1911 (Rangel et al. 1992), experimentally infected insects of this species. Several measurements of insects of this species from localities in the Brazilian states of Espírito Santo, Rio de Janeiro and São Paulo were taken. Insects collected in the winter and in the summer, in one of the localities, were also compared, to check the occurrence of seasonal variation in size (cyclomorphism). The influence of altitude, latitude and season upon the size of this species and their possible relationship to the epidemiology of cutaneous leishmaniasis was analyzed.

The work was developed with specimens collected in the following municipalities: Venda Nova do Imigrante [Espírito Santo (ES), 20^o 20' 23" S 41^o 08' 05" W, 750 m above sea level], Viana (ES, 20^o 23' 25" S 40^o 29' 46" W, 30 m a. s. l.), Cordeiro [Rio de Janeiro (RJ), 21^o 59' 02'' S 42^o 15' 10'' W, 266 m a. s. l.], Petrópolis (RJ, 22^o 15' 14" S 43^o 04' 25" W, 490 m a. s. l.), Cachoeiras de Macacu (RJ, 22^o 27' 45" S 42^o 39' 11" W, 58 m a. s. l.), Itaguaí (RJ, 22^o 51' 08'' S 43^o 46' 01" W, 13 m a. s. l.), Niterói (RJ, 22^o 53' S 43^o 06' 13'' W, 5 m a. s. l.), Parati (RJ, 23^o 13' 04'' S 44^o 42' 47'' W, 5 m a. s. l.), Rio Bonito (RJ, 22^o 42' 30'' S 42^o 37' 34'' W, 62 m a. s. l.), Ubatuba [São Paulo (SP),

23^o 26' 12" S 45^o 04' 16" W, 3 m a. s. l.] and São Sebastião (SP, 23^o 45' 36'' S 45^o 24' 35'' W, 1.4 m a. s. l.).

The samples from Venda Nova do Imigrante, Cordeiro and Petrópolis were considered as coming from high altitude and the others from low altitude. The samples from Venda Nova do Imigrante and Viana were considered as coming from lower latitude and the others from higher latitude. The comparisons related to latitude were made separately for the groups of higher and lower latitude. Samples of insects collected in June and in December 1994 in Venda Nova do Imigrante were compared.

The insects were mounted in NC medium (Nelson Cerqueira, Enecê in Portuguese) (Cerqueira 1943) or using the Berlese method. Modifications in the measurements resulting from the preparation method (Marcondes et al. 1997) were corrected before the statistical analysis was made. Thirty-nine structures and distances, listed by Marcondes (1997), as well as the various ratios between measurements, were established for insects of both sexes.

The data were analysed by ANOVA, with a Confidence Limit of 5% (P<0,05) and 1% (P<0,01) level, using Excel 4.0 program. The Coefficient of Variation was calculated by: C. V.=, where s is the standard deviation and m is the mean, graded from extremely good to extremely bad (Ferreira 1991).

Tables I and ^II show, respectively for females and males from the State of Espírito Santo, the results of insects from higher localities and from lower ones which differed significantly. The specimens of both sexes collected from Venda Nova do Imigrante showed several dimensions greater than those from Viana. Most differences were significant at 1%, probably indicating a positive influence of altitude upon the dimensions.

Tables III and ^IV show the analogous results for females and males from the states of Rio de Janeiro and São Paulo. The length of Antennomere III and of the genital filaments of males and the length of the wings of females were even greater in the insects from the low altitude localities. The variation of the measurements was low; the C.V. exceeded 10% only in some of them, mostly in those of female genitalia.

In comparisons of different altitudes, Tables V and ^VI show the significantly different results between localities of high altitude, for females and males, respectively. Tables VII and ^VIII show the similar results for low altitude localities. In the insects of either sex collected at the low altitude localities, several structure sizes were greater in those from higher latitudes, contrasting with the comparisons from the high altitude localities, in which most dimensions were greater in the insects from Venda Nova do Imigrante. Only the ratio length of wing/maximum width of wing of females was greater in insects from Viana.

Table IX shows the significantly different dimensions of female insects collected in June and in December 1994. No significant differences were noted between dimensions of males, possibly because the number of studied insects of June was small.

The number of differences between the specimens from localities of high altitudes in Rio de Janeiro and those of low altitudes in this State and in São Paulo were smaller than those observed in the comparisons of insects from the state of Espírito Santo. The contrasting result of the genital filaments, Antennomere III and length of wings (Tables III and ^IV ) is probably related to the relatively lower altitude of the "high" localities of Rio de Janeiro, when compared to that of Venda Nova do Imigrante.

The ratio length of wing/length of mesonotum was greater in female insects of high altitude localities of the states of Espírito Santo and Rio de Janeiro than in those from lower altitudes. Comparing the females from high and low altitude localities, this ratio was greater in females from lower latitudes. This ratio was greater in Drosophila melanogaster bred at higher temperatures, and probably influences its flight capability (David et al. 1994). The results obtained from the study of Lu. intermedia indicate a contradictory effect of altitude and of latitude on this ratio, not pointing out a definite influence of temperature for this species.

Considering that there were many significant differences in the comparisons between insects from Venda Nova do Imigrante and those from Viana (Tables I and ^II ), the effect of altitude on structure sizes of Lu. intermedia seems to be much greater than that of the latitude. Possibly, a comparison between insects from localities in the Northeast of Brazil and those of Rio de Janeiro and São Paulo would reveal significantly differences.

The differences between the apparent influence of latitude on the dimensions in different altitudes (Tables VII and ^VII I vs. Tables V and ^VI ) could be caused by the much higher altitude of Venda Nova do Imigrante, compared to those of the localities of Rio de Janeiro, and to the smaller differences of latitude between the localities of higher altitude.

Although the insects collected in June probably developed at lower temperatures than those collected in December, there was no tendency to greater structure sizes among the former. This could be due to stable conditions at the breeding places of sandflies in the locality. Although the conditions of potential breeding places of sandflies were studied at a Panamanian forest (Rutledge & Ellenwood 1975a,b), the relationship between the macroclimatic and microclimatic conditions of these habitats in other environments should be analysed.

Bergmann's rule has been considered as valid for many animals (e. g., Pantelejev 1985, Yon-Tov & Nix 1986), including insects (Cushman et al. 1993, Stone 1993, Sota 1994). However, its validity was refuted (Geist 1987), because the variation in the ratio between the body surface and the volume of mammals was lower than that foreseen by the rule. Most studies of poikilotherms revised by Atkinson (1994) showed a relationship between the rise in the breeding temperature and a reduction in size.

Lane (1988) revised the studies on the relationship between morphometry and various environmental conditions in Old World sandflies. He emphasized the gradients of variation in measurements and counts between forms of sandflies formerly considered distinct. Lane (1988) observed an influence of the breeding temperature of pupae of Lu. longipalpis on some adult dimensions and recommended caution in the use of quantitative characters to differentiate closely related species. The non-applicability of Bergmann's rule to sandflies of the Lu. intermedia complex in the State of São Paulo, in a trial of them as only one species, corroborated the distinction between Lu. intermedia and Lu. neivai (Pinto, 1926) (Marcondes et al. 1998).

Allen's rule, which states that appendages are proportionally longer in colder areas (Lane 1988), could be applicable to Lu. intermedia, with regard to legs, palpi and other appendages, and should be studied using a greater number of intact insects. Gogler's Rule suggests that animals from warm and humid areas are more heavily pigmented than those from cool, dry areas (Lane 1988), as noted for Phlebotomus schwetzi and its variety nigrans (Kirk & Lewis 1951). After establishing a reliable method for the evaluation of pigmentation, the possible validity of this rule for Lu. intermedia should be observed.

Lu. intermedia is strongly suspected as a vector of parasites causing cutaneous leishmaniasis at Viana and other low altitude localities in the State of Espírito Santo, besides being the predominant species at Venda Nova do Imigrante. The occurrence of cutaneous leishmaniasis in this state seems to be limited to 700-750 m a. s. l., although Lu. intermedia can be collected even at 930 m a. s. l. (A Falqueto unpublished data). In Ilha Grande, in the State of Rio de Janeiro, where Lu. intermedia and Lu. migonei were the predominant species and most suspected as vectors, the prevalence of cutaneous leishmaniasis was lower in the higher altitude localities, which were also the least deforested areas (Araujo Filho 1978).

The possible relationship between transmission of parasites of cutaneous leishmaniasis and altitude may be more closely related to factors other than to the size of the insects. The temperature suitable for the evolution of Leishmania in the sandflies (Rioux et al. 1985), the density of the insects and their interaction with reservoirs and human population are some of these factors.

This study invites the conclusion that altitude has a positive influence upon several dimensions and can affect some ratios of Lu. intermedia. Latitude can influence some dimensions, and this should be better studied. Comparative studies on the vectorial efficiency of specimens of this species, bred at different temperatures, would be very useful.

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TABLE I | ^{TABLE II} | TABLE III | ^{TABLE IV} | TABLE V | ^{TABLE VI} | TABLE VII | ^{TABLE VIII} | TABLE IX

⁺Corresponding author. Fax: +55 48 331.9258. E-mail: cbrisola@mbox1.ufsc.br

Received 8 September 1998

Accepted 10 May 1999