Phenology and foraging bias contribute to sex-specific foraging patterns in the rare declining butterfly Argynnis idalia idalia

Abstract

Variation in pollinator foraging behavior can influence pollination effectiveness, community diversity, and plant-pollinator network structure. Although effects of interspecific variation have been widely documented, studies of intraspecific variation in pollinator foraging are relatively rare. Sex-specific differences in resource use are a strong potential source of intraspecific variation, especially in species where the phenology of males and females differ. Differences may arise from encountering different flowering communities, sex-specific traits, nutritional requirements, or a combination of these factors. We evaluated sex-specific foraging patterns in the eastern regal fritillary butterfly (Argynnis idalia idalia), leveraging a 21-year floral visitation dataset. Because A. i. idalia is protandrous, we determined whether foraging differences were due to divergent phenology by comparing visitation patterns between the entire season with restricted periods of male-female overlap. We quantified nectar carbohydrate and amino acid contents of the most visited plant species and compared those visited more frequently by males versus females. We demonstrate significant differences in visitation patterns between male and female A. i. idalia over two decades. Females visit a greater diversity of species, while dissimilarity in foraging patterns between sexes is persistent and comparable to differences between species. While differences are diminished or absent in some years during periods of male-female overlap, remaining signatures of foraging dissimilarity during implicate mechanisms other than phenology. Nectar of plants visited more by females had greater concentrations of total carbohydrates, glucose, and fructose and individual amino acids than male-associated plants. Further work can test whether nutritional differences are a cause of visitation patterns or consequence, reflecting seasonal shifts in the nutritional landscape encountered by male and female A. i. idalia. We highlight the importance of considering sex-specific foraging patterns when studying interaction networks, and in making conservation management decisions for this at-risk butterfly and other species exhibiting strong intraspecific variation.

Keywords: Speyeria idalia idalia; flower visitation; intraspecific variation; long‐term ecological data; nectar chemistry; plant–pollinator interactions; sex‐specific foraging.

FIGURE 1

Observations of female and male floral visitations in the full (a, left) and overlap (b, right) datasets. Ordinal days are defined as day from the start of the year, with January 1 being ordinal day 1. A protandrous life history creates a scenario in which differences between male and female floral visitation differences may be partially explained by phenology. Heights and shapes of peaks represent smoothed number of visitations over time, with heights scaled within year. The overlap dataset (right) considers differences in floral visitation that occur between the first and last weeks of each year wherein females represent at least 25% but no more than 75% of observations. Overlap data for 2009 was limited to a three‐day period while 2001 and 2018 consisted of single day observation periods; these years were therefore removed from subsequent analyses involving the overlap dataset.

FIGURE 2

Dissimilarity of female and male regal fritillary foraging patterns as measured by the Morisita‐Horn dissimilarity index across a 21‐year period. The Morisita–Horn dissimilarity index ranges between 0 and 1; the greater the difference between male‐ and female‐associated plant assemblages, the larger the index value. Observed values (circles) were compared with a distribution of 1000 null model values (triangles) ±95% CI generated by randomizing associations in the community. Blue symbols represent the observed and expected values for the full dataset; orange‐red symbols represent observed and expected values for the overlap dataset. In the full dataset, male‐ and female‐ associated assemblages were more dissimilar than expected by chance in 20 of the 21 years studied. When phenological overlap was considered, overall dissimilarity decreased but remained greater than expected by chance in 9 of 18 years.

FIGURE 3

Sex‐specific associations with plant species visited by eastern regal fritillaries across a span of (a) 21 years in the full dataset comprising the entire season and (b) a restricted period of overlap between male–female flight activity, considering only those 9 years in which we detected a greater Morisita–Horn dissimilarity in the overlap data. Significant differences in visitation bias exist across all years in both datasets. The size of circles and color saturation (scale bars) indicate larger Pearson's Chi‐squared residuals and thus a greater magnitude of deviation from expected values, with red denoting a positive association (i.e., visitation is greater than that expected based on the number of times a foraging event was observed in relation to observations of males and females) and blue denoting negative association. Female and male residuals for each plant species, though similar, are not mirror images; they are a product of both row and column marginal totals and thus can vary independently.

FIGURE 4

Comparisons of nectar carbohydrate concentrations for female (F)‐ versus male (M)‐associated nectar plants. We tested for differences in nectar concentrations of (a) total carbohydrates, (b) glucose, (c) sucrose, (d) maltose, and (e) fructose. Significant differences between male‐ and female‐associated species (p < .0125) are indicated by an asterisk. Data points represent individuals of the six plant species that contributed most to differences between female and male nectar resource use. Open versus filled shapes of the same color indicate congeneric species.

FIGURE 5

Comparisons of nectar amino acid concentrations for female (F)‐ versus male (M)‐associated nectar plants. We tested for differences in nectar concentrations of (a) total amino acids, (b) proline, (c) glycine, and (d) leucine. Significant differences between male‐ and female‐associated species (p < .01) are indicated by an asterisk. Data points represent individuals of the six plant species that contributed most to differences between female and male nectar resource use. Open versus filled shapes of the same color indicate congeneric species.