Offshore renewable developments - developing marine mammal dynamic energy budget models: report

3 Background

Disturbance can cause behavioural, physiological and health changes which can have subsequent effects on an individual’s vital rates, such as survival and reproduction. The cost of disturbance is in most cases mediated by the state of the individual (e.g., life history stage, exposure history), and the environment that the individual is in (e.g., resource availability). By modelling health, we have an explicit scalar link between individual health, response to disturbance, and the consequential population demographic effects of this disturbance (Pirotta et al. 2018a). To date, many PCoD studies have used only changes in an individual’s energy stores (e.g., body condition) as a proxy metric of health (Schick et al. 2013, Nabe-Nielsen et al. 2014, New et al. 2014, Villegas-Amtmann et al. 2015, McHuron et al. 2017, Villegas-Amtmann et al. 2017, Nabe-Nielsen et al. 2018, Pirotta et al. 2018b). To build on this, bioenergetics models also consider the variance in energetic demands on an individual and their associated behavioural and physiological state during different life history stages and take into account the state of the environment the individual is in (e.g., resource density, presence of predators). The role of energy reserves in different reproductive strategies can be thought of as being on a theoretical spectrum relating to how reproduction is fuelled. This spectrum runs between relying solely on capital reserves accrued through the preceding year (capital breeding) through to exclusive reliance on increasing energy intake to cover the increased costs reproduction (income breeding). As with other taxa, marine mammals show a variety of life history patterns, between the ‘capital breeding’ end of the reproductive spectrum (e.g., minke whale, grey seal) through to the ‘income breeding’ end (e.g., harbour porpoise, bottlenose dolphin, harbour seal). The choice of reproductive strategy can have a great impact on the energetic consequences of disturbance, varying each individual’s vulnerability to disturbance based on both its reproductive strategy and stage. Accounting for life history stage and the associated energetic demands in PCoD models means the model can account for how these demands might affect the individual’s response to disturbance. An example of variation in disturbance response based on context would be that a lactating female in a resource poor environment would likely respond very differently to a non-lactating female in a resource-rich environment (Hin et al. 2019).

Bioenergetic models have been used to infer changes in an individual’s energy stores with behavioural state or as a consequence of disturbance (see Table 1 for a comprehensive list of examples), and have been widely used to investigate potential impacts of disturbance (both natural and anthropogenic) on marine mammals at both individual and population level (see Pirotta et al. 2018a for a review). However, many bioenergetic models assess the effects of disturbance on marine mammals by focusing on a single reproductive cycle of a female’s life history (Braithwaite et al. 2015, Christiansen and Lusseau 2015, Villegas-Amtmann et al. 2015, McHuron et al. 2016, Pirotta et al. 2018c). For an in-depth assessment of how disturbance might affect population growth rate over a longer period, it is necessary to model female energetics over the entire lifespan in order to highlight life history stages that are particularly vulnerable to disturbance (Villegas-Amtmann et al. 2017, McHuron et al. 2018, Pirotta et al. 2018a). Hin et al. (2019) used the DEB model presented by De Roos et al. (2009) as a baseline model to simulate the life history of a female pilot whale from weaning age onwards (including during pregnancy and lactation), and for a calf from birth until weaning. Incorporation of this DEB model into a PCoD framework allowed the authors to predict how vulnerability to different disturbances varied with resource availability and life history stage.

3.1 An introduction to DEB models

DEB theory (Nisbet et al. 2000, Kooijman 2010) provides a mechanistic framework that predicts the consequences of an organism’s acquisition of environmental resources for energy demanding traits, such as growth and reproduction, via internal physiological functions. DEB models employ a set of differential or difference equations and parameters that are based on unifying metabolic theory and can theoretically be used to model any species. These equations describe the life history processes of a cohort of organisms, based on energy fluxes. Resources assimilated from the environment are allocated to maintenance, growth and reproduction via a reserve compartment. In the standard DEB model, both structure and reserves contribute to total biomass, but only structure requires maintenance, and all metabolic processes are fuelled from reserves. These two state variables (structure and reserves) can be difficult to measure directly in many species, but they can be linked to more easily observable traits such as body size or age at first reproduction.

3.1.1 DEB models for marine mammals

In many marine mammal species, subcutaneous blubber appears to act as their main energy reserve. The size of this reserve can be estimated directly from dead animals by dissecting out the tissue and weighing it (e.g., Worthy and Lavigne 1987). It can be estimated indirectly using hydrogen isotope dilution techniques (e.g., Costa et al. 1986), although this technique provides an estimate of total body lipid, rather than just blubber. However, blubber performs a number of other functions in marine mammals: it insulates; adjusts buoyancy; defines body shape and streamlines; and acts as a spring (Koopman 2007). In addition, the blubber of beaked whales and sperm whales is largely composed of waxy esters, which are much more difficult to catabolise than the fatty acids that are the main component of most other species’ blubber. As a result, individual marine mammals may not be able to use all of the lipid stored in blubber as an energy reserve without compromising their survival.

The most detailed information on the way in which marine mammals manage their energy reserves comes from studies of fasting seals. Although >90% of the energy required by fasting northern elephant seal (Mirounga angustirostris), harp seal (Pagophilus groenlandicus) and grey seal pups comes from the catabolism of lipids (Worthy and Lavigne 1987, Noren et al. 2003, Bennett et al. 2007), they also obtain energy from the catabolism of lean body tissue. In fact, the decrease in their lean body mass may actually exceed the decrease in the size of their lipid reserves, because lean tissue is mostly comprised of water (Noren et al. 2003). Blubber may be preferentially mobilized if ambient water temperature increases, thus reducing the need for extra insulation (e.g., as documented in fasting harbour seal pups by Muelbert and Bowen 1993). Similarly, lactating females may preferentially catabolize blubber lipids to provide the energy and raw materials for milk production (Costa et al. 1986).

To date, a range of DEB models for marine mammals have been published (either in peer-review or grey literature) and more are currently in development. Klanjscek et al. (2007) developed a DEB model for right whales (Eubalaena spp.). Although their primary concern, as noted above, was to understand the factors that might affect the bioaccumulation of lipophilic toxicants, the same model structure could be used to investigate the effects of disturbance that reduced daily energy intake on reproduction and calf survival. Goedegebuure et al. (2018) developed a DEB model for southern elephant seals (Mirounga leonina) and used it to examine the potential effects of changes in resource availability on breeding success and juvenile survival.

Hin et al. (2019) developed a DEB model for North Atlantic long-finned pilot whales (Globicephala melas), which they used to investigate the effects of disturbance that resulted in reduced energy intake on lifetime reproductive success (i.e., fitness). A subsequent manuscript (Hin et al. 2021) expands this model to consider the effect of density dependence. Hin et al. (2019) found that the calves of females breeding for the first time were particularly sensitive to disturbance, but that all calves – and even lactating females – were at risk as the duration of disturbance increased. Moretti (2019) adapted Hin et al.’s model for Blainville’s beaked whale (Mesoplodon densirostris) and used this model to investigate the potential population consequences of changes in foraging behaviour resulting from exposure to navy sonars. In addition, outputs from DEB models developed for harbour porpoise and Pacific walrus (Odobenus rosmarus) have been used to inform expert elicitations for these species (Booth et al. 2019, Harwood et al. 2019). This model framework has been adapted for a model for harbour porpoise (Harwood et al. 2020) and this report summarises the development of similarly structured DEB models for grey seal, harbour seal, bottlenose dolphin and minke whale.