DOI: 10.5061/dryad.37pvmcvnh
title: Fruit-feeding butterfly populations respond to variation in adult food availability: evidence from longitudinal body mass and abundance data

description: 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. 
description: <strong>Study site and
 model species</strong> 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;
 <em>Charaxes fulvescens</em> (average female wing length 4.95
 cm, male 4.50 cm), <em>Euphaedra alacris</em> (4.71, 3.81 cm),
 and <em>E. medon</em> (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 <em>E. alacris</em>;
 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
 <em>E. alacris</em> and <em>E. medon</em>
 (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: <em>C. fulvescens</em> 230 days, <em>E.
 alacris</em> 253 days, <em>E. medon</em> 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).
 <strong>Weighing
 butterflies</strong> We studied the <em>Euphaedra
 </em>butterflies during August 2001-December 2003, and <em>C.
 fulvescens</em> during August 2001-November 2002, with missing data
 for May, June, July, <br>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 <br>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).
 <strong>Butterfly
 abundance data</strong> 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.
 <strong>Weather and
 fruit availability data</strong>
 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;
 <em>Pouteria altissima, Diospyros abyssinica, Fagaropsis angolensis,
 Ficus sansibarica, F.  sur, F.  exasperata, F. natalensis, Mimusops
 bagshawei, Prunus africana, Strychnos mitis,</em> and
 <em>Uvariopsis congensis</em> (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).
description: Each excel file has a sheet explaining the meaning of column
 headers.