Reproduction, seasonal morphology, and juvenile growth in three Malagasy fruit bats

Abstract

The island nation of Madagascar is home to three endemic species of Old World fruit bat in the family Pteropodidae: Pteropus rufus, Eidolon dupreanum, and Rousettus madagascariensis, all three of which are IUCN Red Listed under some category of threat. Delineation of seasonal limits in the reproductive calendar for threatened mammals can inform conservation efforts by clarifying parameters used in population viability models, as well as elucidate understanding of the mechanisms underpinning pathogen persistence in host populations. Here, we define the seasonal limits of a staggered annual birth pulse across the three species of endemic Madagascar fruit bat, known reservoirs for viruses of high zoonotic potential. Our field studies indicate that this annual birth pulse takes place in September/October for P. rufus, November for E. dupreanum, and December for R. madagascariensis in central-eastern Madagascar where the bulk of our research was concentrated. Juvenile development periods vary across the three Malagasy pteropodids, resulting in near-synchronous weaning of pups for all species in late January-February at the height of the fruiting season for this region. We here document the size range in morphological traits for the three Malagasy fruit bat species, with P. rufus and E. dupreanum among the larger of pteropodids globally and R. madagascariensis among the smaller. All three species demonstrate subtle sexual dimorphism with males being larger than females. We explore seasonal variation in adult body condition by comparing observed body mass with body mass predicted by forearm length, demonstrating that pregnant females add weight during staggered gestation periods and males lose weight during the nutritionally deficit Malagasy winter. Finally, we quantify forearm, tibia, and ear length growth rates in juvenile bats, demonstrating both faster growth and more protracted development times for P. rufus as compared with E. dupreanum and R. madagascariensis. The longer development period for the already-threatened P. rufus further undermines the conservation status of this species as human hunting is particularly detrimental to population viability during reproductive periods. Our work highlights the importance of longitudinal field studies in collecting critical data for mammalian conservation efforts and human public health alike.

Keywords: Eidolon dupreanum; Madagascar; Pteropodidae; Pteropus rufus; Rousettus madagascariensis; fruit bat; morphology; pteropodid; seasonality.

Fig. 1.

(A) Map of field sites and distribution of bat captures for Pteropus rufus, Eidolon dupreanum, and Rousettus madagascariensis in Madagascar. Pie size corresponds to total bats captured at each site: 1,700 in the Districts of Manjakandriana/Moramanga (P. rufus n = 317; E. dupreanum n = 732; R. madagascariensis n = 653), 380 in Ankarana National Park (E. dupreanum n = 172; R. madagascariensis n = 208), 47 in Makira Natural Park (P. rufus n = 15; R. madagascariensis n = 32), and 33 in Mahabo forest (P. rufus n = 19; E. dupreanum n = 14). (B) Gestation and lactation periods across the three Madagascar fruit bat species in the central-eastern Districts of Manjakandriana/Moramanga, calculated from the field data (observed) and reported in the literature (assumed). Respectively, for P. rufus, E. dupreanum, and R. madagascariensis, observed gestation begins on: 7 July, 3 August, and 11 September; birth occurs on: 29 September, 16 November, and 12 December; and lactation ceases on: 21 January, 2 February, and 19 February (Supplementary Data SD1.A).

Fig. 2.

(A) Tibia, and (B) ear length across fruit bat species from the literature (left) and from our Madagascar field data (right), colored by genera according to legend; data are grouped by sex (upper = females, lower = males). Violin plots show range and 25%, 50%, and 75% quantiles for each distribution. (C) Linear regression of log₁₀ body mass (in grams, y-axis) by log₁₀ forearm length (in mm, x-axis) across pteropodids from the literature (left) and from all Madagascar field data (right), colored by genera according to legend; data are grouped by sex (upper = females, lower = males). Solid line corresponds to predictions from the fitted model (R²: all pteropodids, M = 0.96, F = 0.95; Malagasy pteropodids, M = 0.96, F = 0.97). Data are summarized in Supplementary Data SD1.B and SD1.C.

Fig. 3.

Seasonal variation in mass:forearm residual by sex (females = left, males = right) and species. Raw data from central-eastern Madagascar are shown as open circles with prediction from fitted generalized additive model (GAM) as solid line; 95% confidence intervals by standard error are shown by shading surrounding solid line (Supplementary Data SD1.E). For female plots, vertical shading corresponds to the species-specific gestation period; for male plots, vertical shading corresponds to the winter dry season.

Fig. 4.

Variation in juvenile forearm, tibia, and ear length with days since birth, corresponding to the date of first observed juvenile for each of three Madagascar species (29 September for Pteropus rufus, 16 November for Eidolon dupreanum, 12 December for Rousettus madagascariensis). Raw data are plotted as gray shapes (females = triangles, males = circles), with predictions from fitted generalized additive model (GAM) overlain as solid lines; 95% confidence intervals by standard error are shown by translucent shading (Supplementary Data SD1.F). The slope (derivative) of each fitted GAM at day 30 is identified in the bottom right; derivative results across the first year are summarized in Supplementary Data SD1.G.