Studies of population ecology of tropical butterflies are extremely scarce in the literature (see Vlasanek et al. 2013, Vlasanek & Novotny 2015 and references therein), and besides some recent efforts, most published studies of tropical butterflies are restricted to species of Nymphalidae and Papilionidae (e.g. Ramos & Freitas 1999, Freitas et al. 2001, Uehara-Prado et al. 2005, Tufto et al. 2012, Beirão et al. 2012, Vlasanek & Novotny 2015). This general lack of data on dispersal and demography of tropical butterflies hinders our capacity to understand ecology and functioning of plant-insect systems in tropical forests and to propose adequate measures for the conservation of endangered tropical butterflies (Freitas 1996, Freitas & Marini-Filho 2011, Vlasanek et al. 2013).

For Heliconius Kluk (Nymphalidae) butterflies, however, the situation is different. These are by far the most studied tropical butterflies, and concerning population ecology, a relatively large literature is available, including several different species and populations from Florida to Southern Brazil (Turner 1971, Ehrlich & Gilbert 1973, Cook et al. 1976, Araujo 1980, Brown 1981, Mallet & Jackson 1980, Romanowsky et al. 1985, Quintero 1988, Gilbert 1991, Ramos & Freitas 1999, Andrade & Freitas 2005, Sobral-Souza et al. 2015 and references therein). All these studies helped us to construct a general picture about Heliconius population patterns through space and time and to review the early ideas of low-density constant populations, which are typical of those populations from tropical sites (Ramos & Freitas 1999, Andrade & Freitas 2005, Sobral-Souza et al. 2015).

Nevertheless, although Heliconius butterflies are well known in terms of population ecology, published studies are restricted to a dozen of the approximately 40 described species in the genus (see references above), most of them in lowland tropical forest habitats (but see Fleming et al. 2005 for a study in an urban garden in Florida). In fact, most known Heliconius are typical of forested habitats, although some species such as Heliconius erato (Linnaeus) are able to persist in several different vegetation types (Araujo 1980, Ramos & Freitas 1999).

Contrary to its congeners, Heliconius hermathena hermathena (Hewitson) is associated with open vegetal formations, including the white-sand vegetation known locally as “Campina” or “Campinarana” (see detailed description of these habitats in Ducke & Black 1953, Anderson 1981 and Adeney et al. 2016), where the highlight, low- humidity, and often harsh conditions are restrictive for almost all other species of Heliconius (Brown & Benson 1977). In a detailed and extensive study, Brown & Benson (1977) presented comprehensive information on the systematics, biogeography, natural history (including host plant and immature stages) mimicry and ecology of this peculiar species of Heliconius. However, in the above study, demographic data for H. hermathena was restricted to a limited mark-recapture session during a few days, where little population data has been recorded (see Brown & Benson 1977).

The present paper describes the population biology of H. hermathena hermathena (Hewitson, [1854]) in central Amazonia based on a 14-month mark-recapture program. Given the fragile situation of the Amazonian white sand forests (Adeney et al., 2016), the results provide information that could aid in future management of this butterfly species and its fragile and unprotected habitats.

Study Sites and Methods

A mark-release-recapture (MRR) study of Heliconius hermathena hermathena was carried out in the “Parque Zoobotânico das Faculdades Integradas do Tapajós” (02°27′38″S, 54°43′59″W; ca. 25–30 m a.s.l.) (Figs. 1A, B), in the city of Santarém, Pará, Northern Brazil. The study area is covered with a mosaic of “terra firme” (never floodable forest) and open forests in different degrees of succession. Annual rainfall reaches 2100 mm and the average annual temperature is 26°C (INMET 2016) (a climagram for the study area is presented in Fig. 2). Butterflies were marked and recaptured in a trail (1.8 km long, divided into 49 sectors varying from 40 to 100 m, Figs. 1A, B) inside the forest during 14 months, from January 7, 2012 to February 26, 2013, for a total of 107 days (approximately 4 hours/day). Butterflies were netcaptured, individually numbered on the underside of both forewings with a black permanent felt-tipped pen, and released. Characteristics of each individual (wing size, point of capture, sex and food sources) were recorded for later analysis (as in Ramos & Freitas; 1999 and Beirão et al. 2012).

Table 1.

Permanence of males (n = 524) and females (n = 395) of marked H. hermathena hermathena. Days elapsed between marking and last recapture represent the minimum permanence (MP) for each individual.

The MRR data were analyzed using the Joly-Seber method for estimating population parameters (Francini 2010a, b). Males and females were analyzed separately. To estimate the number of individuals present per day, recaptured individuals were considered to be present on all previous days since the first capture (i.e. marked animals at risk, following Freitas & Ramos 2001). Time of permanence in population (i.e. minimum permanence, an indirect measure of longevity) was calculated as days elapsed between marking and last recapture (following Brussard et al. 1974). The sex ratio was calculated through the monthly means of daily proportions in number of individuals captured per day.

Results

Population Dynamics. A total of 2014 individuals of Heliconius hermathena hermathena (1095 males and 919 females) (Figs. 1C, D) were captured between January 2012 and April 2013. The number of individuals captured per day varied from one to 53 for males (mean = 20.9; SD = 10.29; n = 107 d), and from two to 47 for females (mean = 17.2; SD = 7.84; n = 107 d). The number of individuals present per day varied from one to 96 for males (mean = 56.4; SD = 18.38; n = 107 d), and from six to 66 for females (mean = 37.7; SD = 10.78; n = 107 d). The population was constant through the year, with no marked peaks of abundance for both sexes, with females always less abundant (Fig. 3). In general, estimated population numbers were not greater than the number of individuals present per day, especially for females (Fig. 3).

Table 2.

Number of recaptures for all marked individuals of males and females H. hermathena hermathena.

Fig. 1.

A, B. Two views of the trails where the mark-release -recapture study of H. hermathena hermathena had been carried out; C, D. Males of H. hermathena hermathena visiting flowers of Spermacoce capitata (Rubiaceae) and Turnera ulmifolia (Turneraceae), respectively; E. A nocturnal roosting aggregation of H. hermathena hermathena.

Residence Time. The residence time (based on recaptured individuals) varied from two to 139 days for males (mean = 34.9 d; n = 524) and from two to 129 days for females (mean = 30.5 d; n = 395) (Table 1). Life expectancy (following Cook et al. 1967) was 50.8 days for males and 22.5 days for females. Survival curves (following Ehrlich and Gilbert 1973) are similar for both sexes (Kolmogorov - Smirnov test, P > 0.05, df = 2), approaching a type II survival curve (Fig. 4).

Sex Ratio. The sex ratio of individuals captured and marked was male biased (sex ratio of 1.2:1), with 1095 males and 919 females marked (X² = 15.38; df = 1; P < 0.0001), with males dominant in most months (Fig. 5). Both, males and females were recaptured from one to 13 times (Table 2); 524 males (47.9%) and 395 females (42.9%) were recaptured at least once, with males recaptured more than females (X² = 4.78; DF = 1; P = 0.032).

Wing Size. The forewing length ranged from 31.0 to 46.0 mm in males and from 30.0 to 45.0 mm in females. The average forewing length of males (mean = 42.1 mm, SD = 1.74, n = 1094) was greater than that of females (mean = 41.6 mm, SD = 1.69, n = 919) (t = 6.32, df = 2011, P < 0.0001). The mean forewing length of both sexes were constant along the year (Fig. 6).

Fig. 2.

Climatic diagram of the study site (see methods) during the study period (format following Walter 1985). Dotted = dry periods, hatched = humid periods, black = superhumid periods.

Natural history and behavior. In the study area, H. h. hermathena was common and easily observed throughout all the year. The adults were commonly observed near forest edges, flying from close to the ground (0.5–1 m high) to 2–3 m searching for flowers. Flower resources were not quantified but adults were observed visiting five species of flowers as nectar and pollen sources, including species in the family Costaceae (Costus sp.), Rubiaceae (Spermacoce capitata Ruiz & Pav., Fig. 1C), Turneraceae (Turnera ulmifolia L., Fig. 1D), Verbenaceae (Stachytarpheta cayennensis (Rich.)) and Vitaceae (Cissus erosa L. Rich.). Activity started before 0700 h in the morning and ceased around 1730 h in the afternoon; most flower visits were observed from 0800 to 1030 h in the morning, with the activity decreasing after 1200 h in the morning, when temperature became very hot in the study site and all adults moved to the shadow of the vegetation. Adults were observed establishing communal nocturnal roosting aggregations on small shrubs (Fig. 1E). The only reported host plant in the study site was Passiflora hexagonocarpa Barb. Rodr. (Passifloraceae).

Discussion

Besides the distinct ecological requirements of H. hermathena hermathena compared with other studied Heliconius, population parameters here described are similar to those described for other species in the genus, which includes the constant populations through the year and long-lived adults with clear generation overlap (see Turner 1971, Ehrlich & Gilbert 1973, Quintero 1988, Ramos & Freitas 1999).

The male biased sex ratio reported here is a pattern usually reported for butterflies in general and for Heliconius in particular (Mallet & Jackson 1980, Ramos & Freitas 1999, Andrade & Freitas 2005, Herkenhoff et al. 2013, Sobral-Souza et al. 2015 and references therein). Because sex ratios are near to 1:1 in laboratory breeds, behavioral differences between sexes have been suggested as the reason for male biased sex ratios in population studies of tropical butterflies (Ehrlich & Gilbert 1973, Mallet & Jackson 1980, Ehrlich 1984, Freitas 1993, Brown et al. 1995). This is true for most nectar feeding species, where males are more easily captured along trails and forest edges where they come to visit flower resources, while females are supposedly looking for host plants inside the forest (e.g. Freitas 1993, 1996, Ramos & Freitas 1999, Francini et al. 2005). For most heliconians, which are nectar and pollen feeding, behavioral differences among sexes should be responsible for this pattern of male biased sex ratios (see above).

As described for other studied Heliconius, adults of H. hermathena hermathena live about one month on average, with some individuals living up to four months or more. These values are equivalent to those reported for previous studies with Heliconius in both, stable tropical (Turner 1971, Benson 1972, Ehrlich & Gilbert 1973, Quintero 1988, Ramos & Freitas 1999) or seasonal sites (Araujo 1980, Romanowsky et al. 1985, Flemming et al. 2005, Andrade & Freitas 2005). Even considering the small differences reported in previously mentioned studies, present results confirm the general pattern of long adult lifespans of species of Heliconius when compared to other tropical butterflies (Freitas & Ramos 1999, Uehara-Prado et al. 2005). Also in accordance with previous studies, males are more likely to be recaptured and present higher residence times than females, both possibly related to the abovementioned behavioral differences among sexes (see Ramos & Freitas 1999 and references therein).

For tropical butterflies in general, females present greater wing sizes compared to males, a pattern reported in Pieridae (Jones 1992, Vanini et al. 1999, Ruszczyk et al. 2004), Papilionidae (Freitas & Ramos 2001, Beirão et al. 2012, Herkenhof et al. 2013, Scalco et al. 2016), and several groups of Nymphalidae (Kemp & Jones 2001, Uehara-Prado et al. 2005, Francini et al. 2005, Tourinho & Freitas 2009, Cavanzón-Medrano et al. 2016). Conversely, in Heliconius, female biased sexual size dimorphism is rare; males present greater wing lengths than females (Ramos & Freitas 1999 and present study) or differences are not significant (Andrade & Freitas 2005). A notable exception is Heliconius sara (Fabricius) whose males are smaller than females (and territorial advantage is associated with small sizes, see Hernandez & Benson 1998). Femalebiased sexual size dimorphism is the more common pattern for insects in general (Stillwell et al. 2010) and for Lepidoptera in particular (Allen et al. 2011), and is related with larger fecundity in bigger females (Allen et al. 2011 and references therein). Although territorial behavior could partially explain this pattern (see Benson et al. 1989), the reasons for male-biased or no sexual size dimorphism in Heliconius are unknown and a topic to be further investigated.

Fig. 3.

Number of males (above) and females (below) of H. hermathena hermathena from January 2012 to February 2013 in tire study site in Santarém, Pará. Solid circles = number of individuals present per day, open circles = estimated number based on Joly-Seber (bars = 1 standard error).

Fig. 4.

Survivorship curves for H. hermathena hermathena males and females (following Ehrlich and Gilbert 1973). The frequencies of males and females are plotted on log scale against permanence categories (based on data presented on Table 1).

Interestingly, besides the marked seasonality of the study area (with a prominent dry season), the studied population of H. hermathena hermathena was quite constant along the 13 months of study. This pattern is very similar to that reported in non-seasonal sites, such as for Heliconius erato phyllis (Fabricius) in coastal Brazilian Atlantic Forest (Ramos & Freitas 1999) and for Heliconius ethilla (Godart) in Costa Rica (Ehrlich & Gilbert 1973). In seasonal sites, conversely, populations of some species of Heliconius showed marked population fluctuations, with peaks of high densities of adults alternating with periods of extremely low population numbers. This pattern was reported in subtropical sites with a marked cold season, such as Southern Brazil (Araujo 1980, Romanowsky et al. 1985) and Florida (Fleming et al. 2005) and in seasonal forests with a marked dry season (Quintero 1988, Andrade e Freitas 2005). Conversely, Heliconius sara apseudes (Hübner) was reported as strongly seasonal in a stable tropical site in southeastern Brazil (Sobral-Souza et al. 2015).

Based on the present available information, four different population syndromes have been documented for Heliconius: 1) ecologically plastic species occurring in several different habitats, whose populations could be either, constant or seasonal, depending on the local climate—examples are H. erato, H. ethilla (Ehrlich & Gilbert 1973, Ramos & Freitas 1999, Andrade & Freitas 2005) and Heliconius charitonia (L.) (see Cook et al. 1976, Quintero 1988, Gilbert 1991 and Fleming et al. 2005); 2) species presenting marked seasonality independent of the climatic conditions, such as H. sara apseudes (Sobral-Souza et al. 2015, AVLF unpublished); 3) species from cooler montane forests, presenting marked seasonality, such as Heliconius besckei (Ménétriés) (AVLF unpublished) and Heliconius nattereri C. Felder & R. Felder (Brown Jr., K. S., pers. comm.); and 4) specialized tropical species restricted to tropical warm forests, with constant populations even in seasonal sites (such as H. hermathena hermathena in the present study).

Fig. 5.

Sex ratio of H. hermathena hermathena from January 2012 to February 2013 in the study site in Santarém, Pará. Data presented as percent of males (in black) by month (based on means of each days' captures).

Fig. 6.

Mean forewing length of males (solid bars) and females (open bars) of H. hermathena hermathena in the study site in in Santarém, Pará, from January 2012 to February 2013 (based on monthly recruitment). Bars = monthly means, line extensions = standard deviations.

However, information about Heliconius population ecology is limited to very few studies focusing on a restricted subset of less than dozen of the over 40 described species in the genus. Consequently, very few species could be assigned to the above-proposed fourth category, which was for a long time considered as a model of population dynamics in Heliconius. The typical example is H. ethilla; the first studied species of Heliconius from a population point of view and an example of a tropical butterfly with low-density constant populations throughout time (Ehrlich & Gilbert 1973, Ehrlich 1984). Three decades later, Andrade & Freitas (2005) showed that population parameters of the same species (H. ethilla) in a seasonal tropical site with a marked dry period are quite distinct: the population was not constant, showing a marked peak of abundance in the rainy season and a period of extremely low population numbers during most of the dry season.

Gilbert (1991) provided demographic data for eight species of Heliconius, all presenting constant populations in a tropical site in Costa Rica. From these, two of them (H. erato and H. charitonia) were shown to fit in the first population syndrome when additional population data become available (see above). The remaining six species, however, are all restricted to tropical Amazonian and Central American habitats (with one also occurring in the northern tropical portion of Atlantic Forest—Heliconius melpomene (Linnaeus)) and could be good examples of species fitting in the fourth population syndrome (and maybe Heliconius xanthocles H. Bates, see Mallet & Jackson 1980).

In this sense, the present demographic data for H. hermathena hermathena is relevant by adding information that can help in understanding the above proposed population syndromes for the genus Heliconius. In addition, because H. hermathena is a sand forest specialist, it would be important to obtain data from other populations of this same species in different localities in the Amazonia. Finally, understanding the population patterns of this species will add information that can help in future conservation planning for these fragile and potentially threatened habitats.