Estimating reproductive costs in marine mammal bioenergetic models: a review of current knowledge and data availability

Abstract

Reproductive costs represent a significant proportion of a mammalian female's energy budget. Estimates of reproductive costs are needed for understanding how alterations to energy budgets, such as those from environmental variation or human activities, impact maternal body condition, vital rates and population dynamics. Such questions are increasingly important for marine mammals, as many populations are faced with rapidly changing and increasingly disturbed environments. Here we review the different energetic costs that marine mammals incur during gestation and lactation and how those costs are typically estimated in bioenergetic models. We compiled data availability on key model parameters for each species across all six marine mammal taxonomic groups (mysticetes, odontocetes, pinnipeds, sirenians, mustelids and ursids). Pinnipeds were the best-represented group regarding data availability, including estimates of milk intake, milk composition, lactation duration, birth mass, body composition at birth and growth. There were still considerable data gaps, particularly for polar species, and good data were only available across all parameters in 45% of pinniped species. Cetaceans and sirenians were comparatively data-poor, with some species having little or no data for any parameters, particularly beaked whales. Even for species with moderate data coverage, many parameter estimates were tentative or based on indirect approaches, necessitating reevaluation of these estimates. We discuss mechanisms and factors that affect maternal energy investment or prey requirements during reproduction, such as prey supplementation by offspring, metabolic compensation, environmental conditions and maternal characteristics. Filling the existing data gaps highlighted in this review, particularly for parameters that are influential on bioenergetic model outputs, will help refine reproductive costs estimated from bioenergetic models and better address how and when energy imbalances are likely to affect marine mammal populations.

Figure 1

Fat and protein composition (a) and energy density (b) of marine mammal milk. In b, milk energy density was calculated using fat and protein compositions and conversion factors of 39.3 MJ kg⁻¹ (fat) and 24.5 MJ kg⁻¹ (protein). See Supplementary Tables S12-S15 for values and sources.

Figure 2

Mean lactation durations of mysticetes (a) and odontocetes (b), ordered and colored by family. Point estimates represent means from individual studies, with shapes indicating whether data were collected from animals in the wild (circle) or human care (triangle). Line ranges are provided when a range of values was given instead of a single mean, with dashed lines indicating data collected from animals in human care. See Supplementary Tables S17 and S18 for values and sources.

Figure 3

The age (a) or percent time into lactation (b) at which supplemental foraging has been documented in odontocete calves. Shapes and line types indicate whether data are from animals in the wild (circle, solid line) or managed in human care (triangle, dashed line). In b, the percent time into lactation was calculated using average lactation durations (see Fig. 2). When mean lactation duration was a range, we calculated the minimum (earliest age/longest lactation duration) and maximum (oldest age/shortest lactation duration) percent time that feeding likely occurred, with resulting values presented as a range. See Supplementary Table S22 for values and sources.

Figure 4

Data availability for parameters typically used to estimate reproductive costs in marine mammal bioenergetic models in cetaceans (a) and pinnipeds (b), overlaid on a phylogenetic tree. Colors correspond to different data types, with the presence of color indicative of published data (body composition at birth, length or mass at birth, fetal growth curves, milk composition, milk intake rates) or confirmation of specific behaviors (prey supplementation, allonursing; cetaceans only). Missing species labels correspond to species currently recognized as subspecies by the Society for Marine Mammalogy Taxonomic Committee in the June 2021 species list. Currently recognized species not included on the tree are: Rice’s whale (Balaenoptera ricei), Sato’s beaked whale (Berardius minimus), Deraniyagala’s beaked whale (Mesoplodon hotaula), the Indus river dolphin (Platanista minor), and the Indian Ocean humpback dolphin (Sousa plumbea). Phylogenetic tree created using R packages treeio (Wang et al., 2020), ggtree (Yu, 2020), and ggtreeExtra (Xu et al., 2021) using data from the VertLife Project (www.vertlife.org).