Ann. soc. entomol. Fr. (n.s.), 2009, 45 (3) : 265-274

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ARTICLE

Sex-dependent seasonal feeding activity variations among two species of Nymphalidae (Lepidoptera) in the Mexican tropical dry forest

Abstract. Tropical dry forest, such as that found in Mexico, is a biome where very few alimentary resources are available during 6 months of the year. Within some families of Lepidoptera such as Nymphalidae, some species are known to survive the dry season as adults using the few decayed pulp fruits available as a food source. We compared the temporal abundance and sex ratio of two model species, one belonging to the subfamily Charaxinae, found world-wide, and one belonging to the subfamily Biblidinae, endemic to the Americas. We used baited traps to measure feeding frequency of both species to asses monthly temporal resource use curves. The butterfl y frequency of feeding drops dramatically in the dry season for all species-gender, except for females of the Biblidinae species. There are few differences between the sexes in the relative feeding frequency, assimilated to activity pattern, of Charaxinae between the dry and rainy seasons, while the activity pattern of Biblidinae is very different depending on the sex. These results suggest differential consequences on mate choice competition for both species. Females of the Charaxine species showed a use curve nested on the male curve, while for all other pair-wise comparisons between gender-species, the use curves were signifi cantly different. These differences in the temporal foraging pattern could explain at least in part, the coexistence between both sympatric species in the stressful season.

Resumé. Activité saisonnière de nourrissage dépendante du sexe chez deux espèces de Nymphalidae (Lepidoptera) de la forêt tropicale sêche Mexicaine. La forêt tropicale sèche, comme celle que l’on trouve au Mexique, est un biome où très peu de ressources alimentaires sont disponibles durant 6 mois de l’année. Au sein d’une famille de lépidoptères ; les Nymphalidae, certaines espèces dépassent la saison sèche comme imagos en utilisant les rares fruits à pulpe disponible comme nourriture. Nous avons comparé les ressources temporelles et l’abondance de deux espèces modèles, une appartenant à la sous-famille des Charaxinae, qui est distribuée dans tous les continents, et une appartenant à la sous-famille des Biblidinae, restreinte à l’Amérique tropicale. Nos résultats montrent qu’il y a peu de différences d’activité de vol entre sexes chez les Charaxinae entre la saison des pluies et la saison sèche alors que des différences importantes s’observent pour les Biblidinae. Ces résultats suggèrent des stratégies différentes de concurrence pour l’accouplement. La coexistence entre les deux espèces pourrait s’expliquer, au moins en partie, par des différences dans la structure temporelle de la recherche de la nourriture. Keywords: Charaxinae, Biblidinae, Activity patterns, Sexual dimorphism, Tropical dry forest.

Cecilia Torres (1), Marcela Osorio-Beristain (1), Nestor A. Mariano (1) & Luc Legal (2)*

(1) Departamento de Ecologia CEAMISH-Universidad Autonoma del Estado de Morelos, Cuernavaca, Morelos CP: 62209 Mexico(2) ECOLAB, UMR 5245, Université Paul Sabatier Toulouse III, Bât. 4R3, 118 Route de Narbonne, F-31062 Toulouse cedex 9, France

* Corresponding author

E-mail: legal@cict.fr, cecil_ta22@yahoo.com, mosorio@buzon.uaem.mx, nestor@uaem.mxAccepté le 29 juin 2009

It is considered that animals and plants in tropical areas are not subject to strong temporal selection

pressures, as precipitation and temperature show little variation during the year. Th is is in contrast to temperate areas where winter represents a harsh phase in the cycle of most of organisms. Tropical dry forests (TDF) represent an interesting model (Mooney et al. 1995) because whereas the temperature is more or less stable throughout the year, precipitation is seasonally variable, including a dry season free of rain for 6 to

8 months (Trejo & Dirzo 2000; De Leon-Ibarra 2005; see also Fig. 4A). Globally this type of forest is considered to be the most endangered type of tropical vegetation (Masera et al. 1997). In Mexico, this type of forest originally covered up to 60% of the territory (Trejo & Dirzo 2000; Masera et al. 1997), but now less than 30% actually remains as primary or at least moderately conserved forest (Trejo & Dirzo 2000).

Animals and plants exposed to such irregular levels of precipitation have presumably to adapt, and this is probably why most species encountered in the Mexican and Meso-American TDF are endemic (Gentry 1995). Among animals, insects, especially phytophageous lineages, such as Lepidoptera, are particularly interesting to study because they are sensitive to plant diversity (at least at the genus level) and availability during the year

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(Cappuccino & Martin 1997; Zschokke et al. 2000; Novotny & Basset 2005). Most of the Lepidoptera from the TDF survive during the dry season (like northern species during the cold season) as pupae, eggs or more rarely as caterpillars. However, among the family Nymphalidae, some species survive during the most diffi cult season as adults. Strategies to survive the stressful season are widely documented in temperate and cold regions (Pullin & Bale 1989; Nylin 1992) but surprisingly no studies have been carried out in dry tropical areas. Nymphalidae are among the species of Lepidoptera that possess the longest adult stage which can easily exceed 200 days in both temperate and tropical species (Pullin & Bale 1989; Wiklund et al, 2003; Molleman et al. 2007).

Avaibility of resources is a key point of this study; our personal observations were that there were very few pulp fruits in this type of forest (which is unsuitable for monkeys, for example). Most of the trees composing the TDF are Fabaceae (Dorado et al. 2005; Bermudez-Torres K. personal communication). However, every month, one or a few species of tree produce suitable pulp fruits, maintaining a reduced, but permanent resource for fruit-feeding butterfl ies (De Leon-Ibarra 2005; see also Fig. 4B). Competition between Nymphalidae species for the food resources in the TDF is frequent and will be described in a further study.

Th e butterfl y family Nymphalidae contains about 6000 species that have been placed into about 550 genera. Currently these genera are divided into 12 subfamilies and 40 tribes (Wahlberg et al. 2003). Two main adult feeding guilds can be recognized: the nectar feeding and the fruit-feeding (DeVries 1988, Molleman et al. 2005a). Fermented fruits are one of the sources of amino acids with a concentration similar to nectar (Omura & Honda 2000). Female fruit-feeding (or decayed material) butterfl ies use the carbon, oligo-elements and lipids sourced from fruits to ensure their egg production and in some cases these nutrients play a role in longevity (Fischer et al. 2004, Bauerfeind & Fischer 2005, Bauerfeind et al. 2007, Molleman et al. 2008a, Molleman et al. 2008b). Among the numerous subfamilies of Nymphalidae, tropical Charaxinae, Apaturinae, some Satyrinae and Nymphalinae are the most attracted by fruit (Molleman et al. 2005a; Molleman et al. 2007). Th ese latter studies are on African species, but no studies have been carried out on tropical American Nymphalidae species that belong to the endemic subfamily Biblidinae.

In this paper we explore the strategies of Nymphalidae species to survive the dry season, by comparing the temporal activity variations in food resource use by two species from phylogenetically

distant subfamilies (Wahlberg et al. 2003): Charaxinae and Biblidinae. Th e fi rst subfamily is widespread in the world and also well-represented in tropical Africa and Asia, the second is mostly confi ned to tropical America. Two model species (Anaea aidea, (Guérin-Ménéville 1844), Charaxinae and Myscelia cyananthe, (Felder & Felder 1867), Biblidinae) were chosen as they are very common and almost restricted to the TDF type of forest. Th ese two species are recognized as belonging to the same group in relation to habitat association (De la Maza & Soberon 1998). Th ese two species are equally active from 10h00 to 17h00 and cannot be separated on the basis of a diel activity such as described in DeVries et al. (2008). A special emphasis is given to the feeding and activity diff erences between the sexes.

Th e coexistence of both species, particularly during the stressful season, could be explained, at least in part, by the niche diff erentiation at the temporal dimension expressed as seasonal activity and a suspected competition for resources between species. To explore this hypothesis we measured trap abundances. An analysis of overlapping activity curves was used to test whether butterfl y species temporally partition their activity in the TDF.

Th e aims of this study were: (i) To describe and compare the activities of two unrelated species of fruit-feeding Nymphalidae in the particular context of the Tropical Dry Forest. (ii) To relate the observed diff erences of activity with survival strategies in the face of a fully contrasted seasonal humidity level. (iii) To test whether fruit-feeding Nymphalidae do not have the same activity/feeding strategies, with emphasis on gender diff erences.

Material and Methods

Field site

Th e study was conducted during 2005–2006 at the Reserva de la Biosfera Sierra de Huautla in El Limon, Morelos, Central Mexico. Th e study area was a complex mixture of conserved tropical dry forest and secondary vegetation with Fabaceae, Burseraceae, Poaceae and Asteraceae as the principal families. Th e temperature range was 7°C (coldest nights in January) to 38 °C (hottest days in April) with an annual rainfall of 900 mm (Dorado et al. 2005) occurring mainly from June to October. We visited two study sites, 1 km apart with almost identical vegetation and fauna. Both were close to a seasonally fl owing small stream with green vegetation throughout the year. For almost four months (Mid-February to Mid-May), no green vegetation is present except for a few Cactaceae and adapted trees such as the “Cuatecomate” (Crescentia alata, (Kunth, 1819), Bignoniaceae) neither of which are the host-plants of our two model species (Fig. 1). An important point is that during the dry season, there is always, at least, one species of tree bearing fruit, providing a limited but permanent resource for fruit-feeding butterfl ies (De Leon-Ibarra 2005; see also Fig. 4B).

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Experimental design

Th e traps used were developed in Africa (Plantrou 1976) to catch Charaxinae and are now widely used to collect big Nymphalidae and other Lepidoptera families (Molleman et al. 2005b, Hall & Willmott 1999). Two such traps (1.20 m high, diameter 30 cm, platform 40 × 40 cm) were placed 10 m (in order to limit inter-action eff ects) from each other at two diff erent heights (0.5–1.5 m and 6–7 m respectively, Fig. 2) in order to cover the range from the ground to a height of 10–12 m. Th e attraction mixture, placed on the platform, was composed of fermented banana, beer, rum and yeast. To be eff ective the attraction mix-ture had to stay in the sun during the experimental period but without becoming dry. Although no literature exists on the ef-

fi ciency of such type of traps, the experience of one of us (L.L.) led us to estimate that most of the potentially attracted nym-phalids fl ying within, at least, a radius of 4–5 m around the attraction mixture are trapped (some species can escape easily from traps, but not the two species studied here). Females are normally less attracted than males to such traps: according to the amateur literature, our own experience and published data (Molleman et al. 2007), the bias seems to be around 60–65% males versus 40–35% females. Trapping sessions of 3 hours were carried out every 15 days throughout the whole year, normally around the 7th and the 21st of each month. Th e results obtained from 4 traps were then pooled by month.

Figure 1 One of the two studied sites (So called “Camino Belinda”; 18° 32.867’N; 98° 55.984’O 1332m). Top: a photograph taken on the 30 August 2007; bottom: the same zone (slightly diff erent angle) on the 7 March 2008. Th e red arrows indicate the same hill.

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Individual numbers, species and sex identifi cation were recorded at the traps at the end of each 3 hour baited period. Most of the butterfl ies were released after each period of work. Some individuals were collected and frozen for further genetic studies. In order to determine to what extent trap-abundance is aff ected by actual abundance but also to estimate the bias in favor of males with such traps, we did a control study. For this, we collected with a net over 3 hours, all the individuals belonging to both species within 50 m2 around the place where we were normally trapping (In March and August), (Note: so not to bias the results, attraction traps were not set during this counting). Individuals were released at the end of the count.

Species studied

Photographs (in part taken by one of us, L.L.) of these two species including elements of their natural history are available on the web site www.butterfl iesofamerica.com (Warren et al. 2008). Both species feed mostly on rotting fruits on the ground or more rarely on cuts on branches where sap is fl owing.

Anaea aidea (Guérin-Ménéville 1844), Nymphalidae: Charaxinae. Th is species occurs mainly in Mexico even if some individuals have been collected in the USA (California, Arizona, Kansas and South Texas). In the south it has reached the Northwest of Costa Rica (Warren et al. 2008 and personal checking). Th e systematics of this species are not completely clear as some authors have combined it with taxa that occur in the Caribbean Antilles and with the isolated population in Florida (Anaea troglodyta, (Fabricius, 1775)). Th e closely related A. troglodyta, appears to show seasonal polymorphism (Salvato & Hennessey 2003). Comstock (1961) employed the terms “summer” and “winter” morphs to diff erentiate between seasonal forms within the genus. Th e length of photoperiod exposure experienced by the fi fth-instar larvae (several days prior to pupation), as well as the infl uence of seasonal moisture, have been identifi ed as key factors in determining the seasonal forms within Anaea (Riley 1980; 1988; Salvato & Hennessey 2003). Th e species fl ies at a moderate height most of the time, around 2–10 meters (except when feeding on soil), and cannot be considered as a canopy species. Even though it is more common in TDF, some populations occur in rain forest where it is regularly found along the sides of streams. Alimentation used by adults consists of decayed materials (mainly fruits and carrion) and sap from trees. Only males can be rarely seen mud-puddling and exceptionally, adults feed on fl owers (Lantana mainly). Host-plants recorded are in the Euphorbiaceae especially Croton sp. (Warren et al. 2008).

Figure 2 Experimental design “Plantrou” traps. A, during the dry season at a height of 6–7 meters; B, during the rainy season at a height of 0.5–1.5 meters.

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Myscelia cyananthe (Felder & Felder 1867), Nymphalidae: BiblidinaeTh is species is much more local than the former even if its overall distribution is almost identical. A few records exist for the USA (California, Arizona, New Mexico and possibly Texas) and in the south some populations have reached Guatemala. Four sub-species are typically recognized though this number is possibly higher (potential undescribed subspecies, De la Maza, pers. Comm..). Th ese are: Myscelia cyananthe cyananthe: Hidalgo, Colima, Puebla, Veracruz, Oaxaca, Guerrero, Morelos (studied here), Jalisco and Michoacan (rare); Myscelia cyananthe streckeri (Skinner, 1889): Baja California Sur; Myscelia cyananthe skinneri (Mengel, 1894): Sinaloa and Sonora; Myscelia cyananthe diaziana (De la Maza & De la Maza, 1985): Chiapas, (Stanford & Opler 1993). Th is species only inhabits the wet zones of the TDF; it seems to be absent from desert zones and rain forest. Adults are visible throughout the year but there are no indications of the exact number of generations. Th is species likes shade and settles on trees most of the time. Its fl ight is fast and linear like most of the Nymphalidae and it is more common close to sources of water. Th is species is found between 0 to 5 m. Th e only food sources of adults are decayed organic material and sap. Usually males, but rarely females, can be found puddling on mud (Steiner 1990). Th ere are no records of them using nectar from fl owers, or any published reports on the host-plant of this species, but in Central Mexico, we have seen caterpillars on Sapindaceae (Serjania schiedeana (Schltdl. 1844)). All the information collected concerning this species came from various diff erent sources including some internet sites, fi eld books and data relative to similar species (http://www.butterfl iesandmoths.org/species?l=1796, http://www.fl mnh.ufl .edu/lepsoc/search_proc.asp, Brock et al. 2006, Gali & Schwartz, 1983).

Foraging activity overlap

Data on trapped times were categorized into monthly intervals to characterize species/gender-specifi c resource use curves (i.e., temporal use patterns). In this study the number of specimens per month is considered an estimate of their resource use curves Th is approach to assess temporal niche axes has recently received attention at least in other taxa (Adams & Th ibault 2006). Such curves give a quantitative estimation of the feeding activity of butterfl ies along the year. In order to statistically test diff erences in activity patterns, we used the general overlap index adjusted for sample size (GO adj) and specifi c overlap (SO) statistics (Ludwig & Reynolds 1988, Petraitis 1979) to test for signifi cant diff erences in the use curves by each gender of butterfl y species. GO ranges between 0–1, where 1 represents complete overlap of use curves among gender/species and is computed as a weighted average of species’ use curves (see Petraitis 1979). SO is a pair-wise specifi c overlap test among gender/species i and k, representing the probability that the use curve of gender/species i could have been drawn from gender-species k. Th e null hypothesis is that two gender/species completely overlap. SO was calculated between the sexes within species, and between the same sex of diff erent species.

Sex ratio variation during year

To asses the sex ratio variation with time in both species we performed two logistic regressions, fi tting a generalized linear model (GLM), with binomial errors and logit link function.

Counts per month of male and female butterfl ies were included in the model as a dependent variable, and time in month, as an explanatory variable. For the Anaea species we adjusted a linear model, whereas for Myscelia we used a quadratic linear model and quasibinomial errors to correct for overdispersion. Th ese analyses perform weighted regressions that take care of the monthly diff erences in the number of male/female count used to estimate sex proportion (Crawley 2002). Th e analyses were done using R statistical software ver. 2.8.0 (R Development Team 2008).

ResultsA total of 1320 butterfl ies were collected: 408

A. aidea (275 males and 133 females) and 912 M. cyananthe (445 males and 467 females). No signifi cant diff erences were observed between traps at diff erent heights for species and sexes: A. aidea Upper trap: 140 males and 72 females/ Lower traps: 135 males and 61 females, M. cyananthe Upper: 218 males and 225 females/ Lower: 227 males and 242 females.

Figure 3Specimens collected in bait traps. A, Seasonal activity of both sexes of the two species of butterfl ies: Myscelia cyananthe (Mc) and Anaea aidea (Aa) at the Sierra de Huautla biosphera reserve, in the period June 2005–May 2006. Th e columns represent the average activity per month, and the bar one standard error. B, Monthly sex-ratio from the two studied Nymphalidae fruit feeding species Left: Myscelia cyananthe, Right: Anaea aidea.

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this species showed a clear seasonal dimorphism, individuals having been observed in December and in June, periods when the shift between the dry and rainy season forms was observed (Fig. 3B). Th e quantitative niche of temporal activity of females was lower than males but was included in it (SO = 0.96, Fig. 4C). By contrast, the use curve of males was broad and as a consequence signifi cantly diff erent from that of the females (SO = 0.37, Tab. 2, Fig. 4C). Th e sex ratio for A. aidea did not change seasonally as was indicated by non-signifi cant diff erences (GLM, deviance change between the linear model of time and the null model = 0.11, df change = 1, P = 0.742; residual deviance/df = 0.72; Fig. 3B).

Myscelia cyananthe. In contrast to the male bias in the distribution found in Anaea aidea, we collected the same number of males as females throughout the year with M. cyananthe (Fig. 3B). Th is species, like the former one, is more abundant during the rainy season (224 dry season versus 688 rainy season). Both sexes were present in the fi eld all the year but females were more abundant during the dry season (Fig. 3). Males and females showed a very distinct pattern of activity during the year (Fig. 3). Males showed their main seasonal activity during the rainy season and a marked decline in the dry season, while females kept up an almost constant activity throughout the year (Fig. 4C). Indeed, the sex ratio analysis showed a signifi cant bias toward females during the dry season (GLM parameter estimate: constant, t = –4.82, P < 0.001; linear time, t = 4.92, P < 0.001; quadratic time, t = –4.77, P < 0.001; Fig. 3B), in contrast to the pattern found for A. aidea. When we compared the use curves there were signifi cant diff erences between the sexes (SO = 0.73 and SO = 0.58 for male to female and female to male comparisons respectively, Tab. 2).

We also observed that in the dry season, almost all the other Biblidinae (mainly Hamadryas, and Bolboneura, species less abundant in the study area) collected in the traps were females, showing that this diff erential activity pattern may be widespread at the level of the sub-family.

Comparison of the two speciesFrom an examination of the use curves throughout

the year, it turned out that all pair-wise comparisons for SO between species were signifi cantly diff erent (Tab. 2). However two clear general patterns emerge from our butterfl y records; fi rstly the homogeneity of activities variation during year between both sexes of Anaea and the males of Myscelia, independently of the absolute number of individuals collected (Fig. 3B and

Sexes were easy to distinguish in the fi eld (see www.butterfl iesofamerica.com (Warren et al. 2008)).

No signifi cant diff erences were found between traps and direct visual observation in relationship to activity by sexes, in March (dry season) or in August (wet season): A. aidea Fisher’s Exact Test, p = 0.99, chi-squared = 2.94, df = 1, P = 0.086, dry and wet seasons respectively; M. cyananthe: chi-squared = 1.68, df = 1, P = 0.195, chi-squared = 1.16, df = 1, p-value = 0.281, dry and wet seasons respectively.

We observed the very fi rst copulations at the end of the dry season (beginning of April) for Anaea aidea and at the beginning of the rainy season (late April, May) for Myscelia cyananthe (photography available in www.butterfl iesofamerica.com, Warren et al. 2008)).

Anaea aidea. We collected twice as many males as females (Fig. 3B). Th e number of individuals of both sexes was much higher during the rainy season (352 rainy season versus 56 dry season) even if specimens were collected throughout the year (Fig. 3). Th is abundance pattern was confi rmed by visual counting in the fi eld, as this species was around ten times less abundant during the dry season (Tab. 1). Even though

Table 1. Number of individuals observed of Myscelia cyananthe and Anaea aidea during a day in March (Dry season) and in August (Rainy season) in a humid site of the Sierra of Huautla, where Myscelia and Anaea are present throughout the year.

Dry season Rainy season

M. cyanantheMales 8 25Females 18 23

A. aideaMales 3 21Females 1 20

Table 2. General overlap (GO) and gender-species overlap (SO) indices and statistical tests for activity patterns at Sierra de Huautla reserve biosphera (see Material and Methods for statistical details).

General overlap statisticsNo. gender-spp GO Gmin Gadj V P d. f.

4 0.11 0 0.11 5774.7 < 0.0001 33

Specifi c overlap statisticsGender-spp Pair SO U P d. f.Myscelia ♂ Myscelia ♀ 0.73 284.78 < 0.0001 11Myscelia ♀ Myscelia ♂ 0.58 510.15 < 0.0001 11Anaea ♂ Anaea ♀ 0.37 549.54 < 0.0001 11Anaea ♀ Anaea ♂ 0.96 9.71 0.5565 11Myscelia ♂ Anaea ♂ 0.96 40.06 < 0.0001 11Anaea ♂ Myscelia ♂ 0.94 36.20 0.0002 11Myscelia ♀ Anaea ♀ 0.05 2869.16 < 0.0001 11Anaea ♀ Myscelia ♀ 0.80 60.75 < 0.0001 11

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Fig. 4C). Looking at the frequency of occurrence (Fig. 4C), it can be seen that both sexes of Anaea and the males of Myscelia follow a similar annual tendency. Secondly, by contrast, the females of Myscelia showed a very distinct pattern with a quasi constant activity

throughout the year (only a slight decrease during the dry season). Th e diff erences between both species is clear when we compared temporal trends of sex-ratios, which showed a seasonally marked change in M. cyananthe, in contrast to invariant trends in A. aidea.

Figure 4A, Climatic diagram for El Limón in Central México (18º 31’ N – 98 56’ W). Lines represent monthly averages of rainfall and temperature from 20-year records (1971-2000 periods, Mexico National Meteorological Service). Th e striped area in the graph indicates the dry season with hydric defi cit. B, Occurrence of pulp fruits during the year in the area studied. Except for a few rare species all the species present in the studied area are shown in this fi gure (modifi ed from De Leon-Ibarra 2005). C, Plots of use curves of two butterfl y species counted at the Sierra of Huautla biosphera reserve during a year. Mm, Myscelia cyananthe male; Mf, Myscelia cyananthe female; Am, Anaea aidea male; Af, Anaea aidea female. Lines represent adjusted splines functions.

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DiscussionTh e two species studied survive the dry season as

adults, as do many nymphalid species in temperate regions (Pullin & Bale 1989; Nylin 1992). Th is unusual strategy means they have a long lifespan that covers at least 5 to 6 months of the year (Pullin & Bale 1989). Nymphalidae, along with a few species of Pieridae (Gonepteryx sp.), are known to have a much longer adult life than most butterfl ies (Wiklund et al. 1996). In tropical regions, nectarivorous species such as Heliconius charithonia, (L. 1767), live up to 5 months (Dunlap-Pianka et al. 1977, O’Brien et al. 2003). Heliconiinae live as adults throughout the year and are only absent during the coldest month (generally January in Mexico) of the year as it corresponds to a lack of nectariferous fl owers (Dorado et al. 2005). Some Danainae (mostly documented for Danaus plexippus (L. 1758)) are migratory species and have a suffi cient lifespan to carry out their north-south movements (Svärd & Wiklund 1988). As demonstrated recently, African Charaxinae live as adults as long as some decayed materials are present in the fi eld (Molleman et al. 2005a). Among African Nymphalinae and Satyrinae, all the fruit-feeding species have a lifespan that easily exceeds 100 days. Biblidinae have not been documented at all, as all the previous studies were done in Africa where this sub-family does not occur (Molleman et al. 2005a). Some sub-families, such as Morphiinae (including Brassolini and Amathusinae) have not been studied but fi eld occurrences (at least, as observed in Mexico for Brassolini and possibly Morphiini) suggest similar longevity.

Th e two species studied showed a very diff erent pattern of activity during the dry season. Th e population of Anaea aidea showed a drastic reduction, most likely related to the presence of the low amount of food resources, but without changing the rhythm of activity and foraging throughout the year. On the other hand, Myscelia cyananthe totally changed its behavior between the dry and rainy seasons. Th is is clear for both males and females (Fig. 4C).

Anaea aidea showed a very similar ratio of trap collected males/females as the African Charaxinae (Molleman et al. 2007), with systematically twice as many males being collected as females. Th is can be explained by a lower activity of females who stay on, or close to, their host-plant most of the time but also the active territorial activity of males.

Th e long lifespan suggests that surviving mated females are the source of the rainy season generation. As no host-plants are available during the dry season, we concluded that the lifespan of this species is at least 150/180 days. Th is is comparable with the similar

lifespan of some African species in the fi eld (Molleman et al. 2007). Apart from the density drop, and mating at the end of the dry season (such as Anaea andria, (Scudder, 1875), Riley 1988), no special adaptive behavior is observed for this species in relation to the change of season.

During the rainy season, Myscelia cyananthe shows a very similar general tendency to Anaea with no limiting eff ect of food resources, although a more detailed examination shows fi ne-grain resource partitioning between both species over the year. More males (60%) than females (40%) were collected, as in previous studies, even if females were relatively more common than those of Anaea (67 % and 33 % for male and female respectively). We suggest that the behavior of M. cyananthe, which fl ies slightly lower than Anaea, increases the likelihood of the capture of females and could explain the diff erence in the sex ratio between the two species as it is generally observed in the fi eld (DeVries 1988). During the dry season, the density of adults is almost stable for females (compared with the rainy season) but reduced for males. Th is is interesting as we can hypothesise that the males surviving the dry season then reproduce once the fi rst rains arrive. Males showed a gross activity pattern very similar to that of both males and females of Anaea. Females showed a very distinct pattern of activity that lasted throughout the whole year. A sustained foraging activity for this sex can be explained by the necessity to obtain a permanent source of amino-acids for egg maturation (Fischer et al. 2004). A further physiological study is therefore necessary to confi rm this hypothesis and to explain why this phenomenon was not observed for Anaea. Alternatively this contrasting pattern between both species could be explained by reproductive strategy diff erences related to the optimal oviposition time, which in turn could be linked to the phenology of the host plant and/or parasitoid life cycle susceptibility of the caterpillars. It is to be noted that females mated at the very beginning of the most favorable season, as is the case with various Nymphalinae including Polygonia and Inachis genus (Wiklund et al. 2003, Molleman et al. 2005b).

During the rainy season the direct visual observation did not show any diff erence in numbers between species and sexes, which gives us an estimation of the bias with the Plantrou traps that is in agreement with earlier studies (Molleman et al. 2005a, Robacker 2008)

During the dry season, even if a low number of Anaea aidea was collected, the number of males and females are certainly equivalent. By contrast, we found twice as many females as males of Myscelia cyananthe during our fi eld collection. While trapping this species, we collected six times more females than males during

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the same period. Considering that bait traps typically preferentially attract males, the change of behavior between the dry and rainy season for this species is especially marked.

Th erefore, mate choice selection between both species could be very diff erent, with environmental stress playing an important role in selecting surviving males for M. cyananthe (and possibly for other Biblidinae of tropical dry forest), with strong female competition while mating.

Even if a long lifespan is widespread among Nymphalidae, we show here that some species belonging to two separate sub-families possess diff erent survival strategies. Coexistence between both species, particularly during the dry season when food resources are limited, could be explained at least in part by diff erences in the temporal foraging pattern. Other observed diff erences, such as the diff erent patterns of activity between the sexes, are important to understand life history strategies in this very seasonal environment Acknowledgements. Permission for the fi eld work was granted by the Secretaría de Medio Ambiente y Recursos Naturales, and by the Reserva de la Biosfera Sierra de Huautla. John Woodley is greatly thanked for revising the English.

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