The degree to which variation in adult food availability affects the population dynamics of a species depends on its position on the capital-income breeding continuum. The long-lived butterflies that feed on fruits as adults constitute an example of Lepidoptera with a high degree of income breeding. For three species of fruit-feeding butterflies in Uganda, we assessed the contribution of the income to breeding in the wild, and the consequences of variation in fruit availability for body mass and population dynamics. We interpreted body mass loss within individuals as well as younger individuals having higher body mass than older ones as evidence for the depletion of capital reserves. Despite large sample sizes, we were able to show only modest body mass loss in one species, indicating that large-bodied fruit-feeding butterflies are functionally income breeders in the wild. Butterfly body mass was sensitive to environmental factors, although the responses to fruit availability and weather parameters were dominated by interactive effects. In all three species, periods of higher availability of fruit were followed by periods of higher adult abundance three to five months later, fitting the egg-to-adult time. Our results suggest that adult food is rapidly used for reproduction so that body mass remains stable and population size responds to adult food availability. For these income breeding species, the frequent periods of low adult food availability may select for extended adult longevity for the purpose of postponing reproduction to the onset of more favorable conditions. 

Study site and model species

This study was performed at Makerere University Biological Field Station in Kibale National Park, Western Uganda (0°13’ - 0°41’N and 30°19’ - 30°32’E), a sub-montane tropical forest which has  two rainy seasons per year, while temperature has a unimodal distribution (Valtonen et al. 2013). Kibale is a midaltitude, moist-evergreen forest with over 350 species of tree, many of which bear fruits (Chapman et al. 2010; Chapman et al. 2021). There is significant temporal variation in fruit availability (Chapman et al. 2018; Potts et al. 2020), which has been shown to affect the reproductive function of an income-breeding mammal (Thompson & Wrangham 2008).

We focused on three large-bodied fruit-feeding nymphalid butterfly species that are common in Kibale forest; Charaxes fulvescens (average female wing length 4.95 cm, male 4.50 cm), Euphaedra alacris (4.71, 3.81 cm), and E. medon (4.23, 3.37 cm; Valtonen et al. 2013; Molleman et al. 2020). Dietary restriction studies with wild-caught individuals have shown that females of all three species can use amino acids from income for egg production (Molleman et al. 2008a; Molleman et al. 2009b), and that males (but not females) live longer when provided with amino acids in their diet (Molleman et al. 2009a). However, there are also indications for some degree of capital breeding. All species are able to lay some eggs on sugar-only diets, and they show a decrease in reproductive rate with age even on a fruit diet (especially in E. alacris; Molleman et al. 2009b). Given the high degree of income breeding with regard to amino acids, they are most likely mainly income breeding with respect to carbohydrates, similar to a small-bodied fruit-feeding butterfly species (Fischer, O'Brien & Boggs 2004; Molleman et al. 2008b). Egg-laying occurs throughout the year: caterpillars of these species can be found during any month (unpublished data), and adult abundance does not show seasonality (Appendix 1). While the fruit-feeding butterfly community as a whole responds to rainfall (Valtonen et al. 2013), out of the three study species, a population response to rainfall was only detected in E. alacris and E. medon (Appendix 1). All three species are understory specialists (Molleman et al. 2006) that can fly rapidly (Molleman et al. 2020), have small spermatophores (Molleman et al. 2005a), are long-lived (longevity records: C. fulvescens 230 days, E. alacris 253 days, E. medon 293 days; Molleman et al. 2007), and occur throughout the year with non-seasonal abundance fluctuations (Valtonen et al. 2013; Appendix 1). They have been observed feeding on a variety of fruits, but may also feed on other substances such as sap oozing from trees (Molleman et al. 2005b).

Weighing butterflies

We studied the Euphaedra butterflies during August 2001-December 2003, and C. fulvescens during August 2001-November 2002, with missing data for May, June, July,
and October 2002 (Figure 1). Butterflies were collected from banana-baited traps between noon and 3.30 pm within one km from the field station (for trap location details see Molleman et al. 2006), and kept in cages with up to 10 individuals in a ventilated room. In an attempt to ensure that their gut no longer contained banana bait and that they were satiated with water when weighing, butterflies were provided with moistened tissue paper only, and were weighed the next morning between 8:00 and 8.30 am. Butterflies were weighed inside a glassine envelope on a microbalance. Wing length was measured by holding one forewing to a ruler from wing-base to wing-tip. Wing wear was graded as pristine, slight, intermediate, severe, or very severe; the gradation was collapsed to just two categories (young/old) for the purpose of this study (Appendix 1). Butterflies were marked with a unique number on the ventral side of the forewing using a felt-tipped pen (Staedtler permanent marker). After weighing, butterflies were kept in cages with fresh mashed banana for one hour to avoid harm due to imposed starvation, and were then released into the middle of the study area.

Recaptured butterflies were weighed using the same procedure. Butterflies that were last weighed less than a week ago were generally released from traps without weighing
because little body mass change was expected within a few days. Marking of butterflies took place primarily during trapping for butterfly population monitoring, while recaptures were taken at any opportunity in the course of trapping studies (Molleman et al. 2005a; Molleman et al. 2005b; Molleman et al. 2006; Molleman et al. 2007).

Butterfly abundance data

We used published data on fruit-feeding butterfly abundance obtained through monthly trapping with banana-baited traps (Valtonen et al. 2013). In short, butterflies were counted and released from 22 trap locations for four days once every four weeks for twelve years.

Weather and fruit availability data

Rainfall and daily maximum and minimum temperature data were obtained from a weather station at the site during the study period (Chapman et al. 2018). We calculated average daily temperature as the mean of the minimum and maximum temperature. Over the study, average daily rainfall over 30-day periods was 4.9 mm ranging from 0.1 to 14.6 mm per day (Figure 1A). The mean of 30-day daily average temperatures was 21.1℃, ranging from 18.6 to 22.3 ℃. The mean of 30-day average maximum temperatures was 26.0 ℃, ranging from 23.3 to 30.1℃ (Figure 1B).

To derive an index of the abundance of adult food, we used published fruiting phenology data from the study site, based on a set of labeled fruit-bearing trees that had been monitored monthly during the study period (Chapman et al. 2018). For our analyses, we selected only those tree species that produce fruits on which butterflies feed, being; Pouteria altissima, Diospyros abyssinica, Fagaropsis angolensis, Ficus sansibarica, F.  sur, F.  exasperata, F. natalensis, Mimusops bagshawei, Prunus africana, Strychnos mitis, and Uvariopsis congensis (Molleman et al. 2005b). As our measure of fruit availability, for each month, we summed the diameter at breast height (DBH) of all the monitored trees with ripe fruits, assuming that larger trees produce more fruits (Chapman et al. 1992; Caillaud et al. 2010; Minor & Kobe 2019). This sum within a sample month averaged 603 cm, and ranged from 0 (no monitored tree was bearing fruit) to 1388 cm (Figures 1C & 6A).

Each excel file has a sheet explaining the meaning of column headers.