Dynamic energy budgets and bioaccumulation : a model for marine mammals and marine mammal populations

Submitted to the Department of Biology in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Biological Oceanography at the Massachusetts Institute of Technology and the Woods Hole Oceanographic Institution June 2006Energy intake of individuals affects growth of organisms and, therefore, populations. Persistent lipophilic toxicants acquired with the energy can bioaccumulate and harm individuals. Marine mammals are particularly vulnerable because of their large energy requirements, and transfer of energy and toxicants from mothers to their young during gestation and lactation. Dynamic energy budget (DEB) models for energy assimilation and utilization, coupled with pharmacokinetic models that calculate distribution of toxicants in individuals, can help investigate the vulnerability. In this dissertation I develop the first individual DEB model tailored specifically to marine mammals and couple it to a pharmacokinetic model for lipophilic toxicants. I adapt the individual model to the right whale and use it to analyze consequences of energy availability on individual growth, reproduction, bioaccumulation, and transfer of toxicants between generations. From the coupled model, I create an individual-based model (IBM) of a marine mammal population. I use it to investigate how interactions of food availability, exposure to toxicants, and maternal transfer of toxicants affect populations. I also present a method to create matrix population models from a general DEB model to alleviate some of the drawbacks of the IBM approach.This work has been supported by the David and Lucile Packard Foundation, the US National Science foundation (DEB-9973518 and OCE-0083976), the US Environmental Protection Agency (R-82908901-0), the National Oceanographic and Atmospheric Administration (NAO 3NMF4720491) and the WHOI/MIT Joint Program in Oceanography

A model for energetics and bioaccumulation in marine mammals with applications to the right whale

Author Posting. © Ecological Society of America, 2007. This article is posted here by permission of Ecological Society of America for personal use, not for redistribution. The definitive version was published in Ecological Applications 17 (2007): 2233–2250, doi:10.1890/06-0426.1.We present a dynamic energy budget (DEB) model for marine mammals, coupled with a pharmacokinetic model of a lipophilic persistent toxicant. Inputs to the model are energy availability and lipid-normalized toxicant concentration in the environment. The model predicts individual growth, reproduction, bioaccumulation, and transfer of energy and toxicant from mothers to their young. We estimated all model parameters for the right whale; with these parameters, reduction in energy availability increases the age at first parturition, increases intervals between reproductive events, reduces the organisms' ability to buffer seasonal fluctuations, and increases its susceptibility to temporal shifts in the seasonal peak of energy availability. Reduction in energy intake increases bioaccumulation and the amount of toxicant transferred from mother to each offspring. With high energy availability, the toxicant load of offspring decreases with birth order. Contrary to expectations, this ordering may be reversed with lower energy availability. Although demonstrated with parameters for the right whale, these relationships between energy intake and energetics and pharmacokinetics of organisms are likely to be much more general. Results specific to right whales include energy assimilation estimates for the North Atlantic and southern right whale, influences of history of energy availability on reproduction, and a relationship between ages at first parturition and calving intervals. Our model provides a platform for further analyses of both individual and population responses of marine mammals to pollution, and to changes in energy availability, including those likely to arise through climate change.This research was supported by the David and Lucile Packard Foundation, the U.S. National Science Foundation (DEB-9973518 and OCE-0083976), the U.S. Environmental Protection Agency (R-82908901-0), NOAA grant NA03NMF4720491, and the WHOI/MIT Joint Program in Oceanography

A full lifecycle bioenergetic model for bluefin tuna.

We formulated a full lifecycle bioenergetic model for bluefin tuna relying on the principles of Dynamic Energy Budget theory. Traditional bioenergetic models in fish research deduce energy input and utilization from observed growth and reproduction. In contrast, our model predicts growth and reproduction from food availability and temperature in the environment. We calibrated the model to emulate physiological characteristics of Pacific bluefin tuna (Thunnus orientalis, hereafter PBT), a species which has received considerable scientific attention due to its high economic value. Computer simulations suggest that (i) the main cause of different growth rates between cultivated and wild PBT is the difference in average body temperature of approximately 6.5uC, (ii) a well-fed PBT individual can spawn an average number of 9 batches per spawning season, (iii) food abundance experienced by wild PBT is rather constant and sufficiently high to provide energy for yearly reproductive cycle, (iv) energy in reserve is exceptionally small, causing the weight-length relationship of cultivated and wild PBT to be practically indistinguishable and suggesting that these fish are poorly equipped to deal with starvation, (v) accelerated growth rate of PBT larvae is connected to morphological changes prior to metamorphosis, while (vi) deceleration of growth rate in the early juvenile stage is related to efficiency of internal heat production. Based on these results, we discuss a number of physiologica

Demographic analysis of continuous-time life-history models

I present a computational approach to calculate the population growth rate, its sensitivity to life-history parameters and associated statistics like the stable population distribution and the reproductive value for exponentially growing populations, in which individual life history is described as a continuous development through time. The method is generally applicable to analyse population growth and performance for a wide range of individual life-history models, including cases in which the population consists of different types of individuals or in which the environment is fluctuating periodically. It complements comparable methods developed for discrete-time dynamics modelled with matrix or integral projection models. The basic idea behind the method is to use Lotka's integral equation for the population growth rate and compute the integral occurring in that equation by integrating an ordinary differential equation, analogous to recently derived methods to compute steady-states of physiologically structured population models. I illustrate application of the method using a number of published life-history models

Sublethal toxicant effects with dynamic energy budget theory: model formulation

We develop and test a general modeling framework to describe the sublethal effects of pollutants by adding toxicity modules to an established dynamic energy budget (DEB) model. The DEB model describes the rates of energy acquisition and expenditure by individual organisms; the toxicity modules describe how toxicants affect these rates by changing the value of one or more DEB parameters, notably the parameters quantifying the rates of feeding and maintenance. We investigate four toxicity modules that assume: (1) effects on feeding only; (2) effects on maintenance only; (3) effects on feeding and maintenance with similar values for the toxicity parameters; and (4) effects on feeding and maintenance with different values for the toxicity parameters. We test the toxicity modules by fitting each to published data on feeding, respiration, growth and reproduction. Among the pollutants tested are metals (mercury and copper) and various organic compounds (chlorophenols, toluene, polycyclic aromatic hydrocarbons, tetradifon and pyridine); organisms include mussels, oysters, earthworms, water fleas and zebrafish. In most cases, the data sets could be adequately described with any of the toxicity modules, and no single module gave superior fits to all data sets. We therefore propose that for many applications, it is reasonable to use the most general and parameter sparse module, i.e. module 3 that assumes similar effects on feeding and maintenance, as a default. For one example (water fleas), we use parameter estimates to calculate the impact of food availability and toxicant levels on the long term population growth rate

Predicting climate change impacts on polar bear litter size

Predicting the ecological impacts of climate warming is critical for species conservation. Incorporating future warming into population models, however, is challenging because reproduction and survival cannot be measured for yet unobserved environmental conditions. In this study, we use mechanistic energy budget models and data obtainable under current conditions to predict polar bear litter size under future conditions. In western Hudson Bay, we predict climate warming-induced litter size declines that jeopardize population viability: ∼28% of pregnant females failed to reproduce for energetic reasons during the early 1990s, but 40–73% could fail if spring sea ice break-up occurs 1 month earlier than during the 1990s, and 55–100% if break-up occurs 2 months earlier. Simultaneously, mean litter size would decrease by 22–67% and 44–100%, respectively. The expected timeline for these declines varies with climate-model-specific sea ice predictions. Similar litter size declines may occur in over one-third of the global polar bear population

Quantifying research waste in ecology

Research inefficiencies can generate huge waste: evidence from biomedical research has shown that most research is avoidably wasted and steps have been taken to tackle this costly problem. Although other scientific fields could also benefit from identifying and quantifying waste and acting to reduce it, no other estimates of research waste are available. Given that ecological issues interweave most of the United Nations Sustainable Development Goals, we argue that tackling research waste in ecology should be prioritized. Our study leads the way. We estimate components of waste in ecological research based on a literature review and a meta-analysis. Shockingly, our results suggest only 11–18% of conducted ecological research reaches its full informative value. All actors within the research system—including academic institutions, policymakers, funders and publishers—have a duty towards science, the environment, study organisms and the public, to urgently act and reduce this considerable yet preventable loss. We discuss potential ways forward and call for two major actions: (1) further research into waste in ecology (and beyond); (2) focused development and implementation of solutions to reduce unused potential of ecological research