Population Consequences of Disturbance

Anthropogenic sounds might affect the behavior and physiology of individual animals. These effects may have short- or long-term changes that could affect individual survival or reproduction, resulting in population changes (e.g., feeding or breeding affecting growth rate or population structure). A conceptual framework, termed the Population Consequences of Acoustic Disturbance (PCAD) model[1]National Research Council (U.S.), & National Academies Press (U.S.) (Eds.). (2005). Marine mammal populations and ocean noise: Determining when noise causes biologically significant effects. National Academies Press. https://doi.org/10.17226/11147, was proposed to understand the population-level effects arising from short-term behavioral changes in response to sound exposure. It is a conceptual model that proposes relationships that are just beginning to be demonstrated with select species. To date, much of the PCAD work has focused on marine mammal populations.

A newer model, Population Consequences of Disturbance (PCoD)[2]New, L., Clark, J., Costa, D., Fleishman, E., Hindell, M., Klanjšček, T., Lusseau, D., Kraus, S., McMahon, C., Robinson, P., Schick, R., Schwarz, L., Simmons, S., Thomas, L., Tyack, P., & Harwood, J. (2014). Using short-term measures of behaviour to estimate long-term fitness of southern elephant seals. Marine Ecology Progress Series496, 99–108. https://doi.org/10.3354/meps10547[3]Committee on the Assessment of the Cumulative Effects of Anthropogenic Stressors on Marine Mammals, Ocean Studies Board, Division on Earth and Life Studies, & National Academies of Sciences, Engineering, and Medicine. (2017). Approaches to Understanding the Cumulative Effects of Stressors on Marine Mammals (p. 23479). National Academies Press. https://doi.org/10.17226/23479[4]Pirotta, E., Booth, C. G., Costa, D. P., Fleishman, E., Kraus, S. D., Lusseau, D., Moretti, D., New, L. F., Schick, R. S., Schwarz, L. K., Simmons, S. E., Thomas, L., Tyack, P. L., Weise, M. J., Wells, R. S., & Harwood, J. (2018). Understanding the population consequences of disturbance. Ecology and Evolution8(19), 9934–9946. https://doi.org/10.1002/ece3.4458[5]Booth, C. G., Sinclair, R. R., & Harwood, J. (2020). Methods for Monitoring for the Population Consequences of Disturbance in Marine Mammals: A Review. Frontiers in Marine Science7, 115. https://doi.org/10.3389/fmars.2020.00115, incorporates multiple disturbances in addition to acoustic exposures (shown in the figure below from Pirotta et al., 2018). An animal is exposed to a stressor, which might result in a physiological or behavioral change. These changes can result in immediate, acute effects (e.g., increased predation or injury resulting in mortality), or long term, chronic effects (reduced fat reserves or energy stores, increased stress or parasite load), both of which may affect population vital rates (e.g., adult or offspring survival, an adult’s fertility).

Effects can also be cumulative and further affect the overall population dynamics. An individual may be exposed to multiple stressors, each of which may result in a physiological or behavioral change that impact its vital rates. Similarly, multiple individuals within the population may be exposed to same stressors, as indicated by the gray dashed rectangles in the figure. The changes to the vital rates of each individual are then aggregated to determine the overall impact on the population[6]Committee on the Assessment of the Cumulative Effects of Anthropogenic Stressors on Marine Mammals, Ocean Studies Board, Division on Earth and Life Studies, & National Academies of Sciences, Engineering, and Medicine. (2017). Approaches to Understanding the Cumulative Effects of Stressors on Marine Mammals (p. 23479). National Academies Press. https://doi.org/10.17226/23479[7]Pirotta, E., Booth, C. G., Costa, D. P., Fleishman, E., Kraus, S. D., Lusseau, D., Moretti, D., New, L. F., Schick, R. S., Schwarz, L. K., Simmons, S. E., Thomas, L., Tyack, P. L., Weise, M. J., Wells, R. S., & Harwood, J. (2018). Understanding the population consequences of disturbance. Ecology and Evolution8(19), 9934–9946. https://doi.org/10.1002/ece3.4458.

Diagram showing the factors and relationships for the conceptual framework of population consequences.
The conceptual framework for population consequences of exposure to multiple stressors includes multiple individuals and population-level consequences. Figure from Pirotta, E., Booth, C. G., Costa, D. P., Fleishman, E., Kraus, S. D., Lusseau, D., Moretti, D., New, L. F., Schick, R. S., Schwarz, L. K., Simmons, S. E., Thomas, L., Tyack, P. L., Weise, M. J., Wells, R. S., & Harwood, J. (2018). Understanding the population consequences of disturbance. Ecology and Evolution, 8(19), 9934–9946. https://doi.org/10.1002/ece3.4458. CC Attribution 4.0 International.

The PCoD model has been applied to real-world, case studies for several subpopulations for which there are extensive data (e.g., demographics and survivorship). Examples include northern and southern elephant seals[8]New, L., Clark, J., Costa, D., Fleishman, E., Hindell, M., Klanjšček, T., Lusseau, D., Kraus, S., McMahon, C., Robinson, P., Schick, R., Schwarz, L., Simmons, S., Thomas, L., Tyack, P., & Harwood, J. (2014). Using short-term measures of behaviour to estimate long-term fitness of southern elephant seals. Marine Ecology Progress Series496, 99–108. https://doi.org/10.3354/meps10547[9]Costa, D. P., Schwarz, L., Robinson, P., Schick, R. S., Morris, P. A., Condit, R., Crocker, D. E., & Kilpatrick, A. M. (2016). A Bioenergetics Approach to Understanding the Population Consequences of Disturbance: Elephant Seals as a Model System. In A. N. Popper & A. Hawkins (Eds.), The Effects of Noise on Aquatic Life II (Vol. 875, pp. 161–169). Springer New York. https://doi.org/10.1007/978-1-4939-2981-8_19, common bottlenose dolphins[10]New, L. F., Harwood, J., Thomas, L., Donovan, C., Clark, J. S., Hastie, G., Thompson, P. M., Cheney, B., Scott‐Hayward, L., & Lusseau, D. (2013). Modelling the biological significance of behavioural change in coastal bottlenose dolphins in response to disturbance. Functional Ecology27(2), 314–322. https://doi.org/10.1111/1365-2435.12052[11]Pirotta, E., Harwood, J., Thompson, P. M., New, L., Cheney, B., Arso, M., Hammond, P. S., Donovan, C., & Lusseau, D. (2015). Predicting the effects of human developments on individual dolphins to understand potential long-term population consequences. Proceedings of the Royal Society B: Biological Sciences282(1818), 20152109. https://doi.org/10.1098/rspb.2015.2109[12]Reed, J., Harcourt, R., New, L., & Bilgmann, K. (2020). Extreme Effects of Extreme Disturbances: A Simulation Approach to Assess Population Specific Responses. Frontiers in Marine Science7, 519845. https://doi.org/10.3389/fmars.2020.519845, North Atlantic right whales[13]Schick, R. S., Kraus, S. D., Rolland, R. M., Knowlton, A. R., Hamilton, P. K., Pettis, H. M., Kenney, R. D., & Clark, J. S. (2013). Using Hierarchical Bayes to Understand Movement, Health, and Survival in the Endangered North Atlantic Right Whale. PLoS ONE8(6), e64166. https://doi.org/10.1371/journal.pone.0064166[14]Rolland, R., Schick, R., Pettis, H., Knowlton, A., Hamilton, P., Clark, J., & Kraus, S. (2016). Health of North Atlantic right whales Eubalaena glacialis over three decades: From individual health to demographic and population health trends. Marine Ecology Progress Series542, 265–282. https://doi.org/10.3354/meps11547, migrating humpback whales[15]Dunlop, R. A., Braithwaite, J., Mortensen, L. O., & Harris, C. M. (2021). Assessing Population-Level Effects of Anthropogenic Disturbance on a Marine Mammal Population. Frontiers in Marine Science8, 624981. https://doi.org/10.3389/fmars.2021.624981, and blue whales[16]Pirotta, E., Mangel, M., Costa, D. P., Goldbogen, J., Harwood, J., Hin, V., Irvine, L. M., Mate, B. R., McHuron, E. A., Palacios, D. M., Schwarz, L. K., & New, L. (2019). Anthropogenic disturbance in a changing environment: Modelling lifetime reproductive success to predict the consequences of multiple stressors on a migratory population. Oikos128(9), 1340–1357. https://doi.org/10.1111/oik.06146[17]Pirotta, E., Booth, C. G., Cade, D. E., Calambokidis, J., Costa, D. P., Fahlbusch, J. A., Friedlaender, A. S., Goldbogen, J. A., Harwood, J., Hazen, E. L., New, L., & Southall, B. L. (2021). Context-dependent variability in the predicted daily energetic costs of disturbance for blue whales. Conservation Physiology9(1), coaa137. https://doi.org/10.1093/conphys/coaa137.

One of the first major studies using the PCoD model was for elephant seal populations. Elephant seals are “capital breeders” meaning they go on extended foraging trips during which they build lipid (fat) stores required for extended haul-out (fasting) periods when females give birth, nurse their pups to weaning, and mate. Long-term telemetry studies have provided an extensive dataset on diving, movement, and foraging behaviors while at sea, and body morphometric measurements at the haul-out sites provide information on the fitness of many individuals in the population. Maternal fitness can be estimated by lipid body content (i.e., the fatter a mom is, the healthier she is, and ultimately her pup will be healthier as well). Maternal lipid mass is directly correlated with the probability of pupping, the pup’s lipid mass, and the pup’s probability of survival[18]Costa, D. P., Schwarz, L., Robinson, P., Schick, R. S., Morris, P. A., Condit, R., Crocker, D. E., & Kilpatrick, A. M. (2016). A Bioenergetics Approach to Understanding the Population Consequences of Disturbance: Elephant Seals as a Model System. In A. N. Popper & A. Hawkins (Eds.), The Effects of Noise on Aquatic Life II (Vol. 875, pp. 161–169). Springer New York. https://doi.org/10.1007/978-1-4939-2981-8_19. Therefore, a disturbance that reduces adult female foraging could decrease the lipid mass of mothers, which could have population-level consequences.

Researchers used models to estimate how a disturbance on elephant seals affects their foraging. If female foraging is decreased at sea by a hypothetical 50%, their mean lipid mass decreased, resulting in decreased pup mass and survival (New et al., 2014). When the model simulated a 30-year period (i.e., for 30 years, the seals were disturbed and there was no foraging for 50% of their time at sea), and the population did not alter foraging behavior, the population declined by approximately 10%.

Much more data on foraging patterns, life history, and demographic information are needed to apply the PCoD model to most marine species, which may take decades to acquire. In addition, research on the variation of responses by individuals within a population are critical to understanding how stresses might accumulate and/or interact. Researchers reviewed existing data on individual responses to changing environmental stressors and found significant differences among individuals based on intrinsic characteristics (e.g., body size, condition, sex, and personality) and extrinsic factors (e.g., environmental context, repeated exposure, prior experience, and multiple stressors)[19]Harding, H. R., Gordon, T. A. C., Eastcott, E., Simpson, S. D., & Radford, A. N. (2019). Causes and consequences of intraspecific variation in animal responses to anthropogenic noise. Behavioral Ecology30(6), 1501–1511. https://doi.org/10.1093/beheco/arz114. Modeling studies are also being done to determine which variables are most important to inform data gaps and provide the best application of the PCoD framework[20]Pirotta, E., Booth, C. G., Costa, D. P., Fleishman, E., Kraus, S. D., Lusseau, D., Moretti, D., New, L. F., Schick, R. S., Schwarz, L. K., Simmons, S. E., Thomas, L., Tyack, P. L., Weise, M. J., Wells, R. S., & Harwood, J. (2018). Understanding the population consequences of disturbance. Ecology and Evolution8(19), 9934–9946. https://doi.org/10.1002/ece3.4458.

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Cited References

Cited References
1 National Research Council (U.S.), & National Academies Press (U.S.) (Eds.). (2005). Marine mammal populations and ocean noise: Determining when noise causes biologically significant effects. National Academies Press. https://doi.org/10.17226/11147
2, 8 New, L., Clark, J., Costa, D., Fleishman, E., Hindell, M., Klanjšček, T., Lusseau, D., Kraus, S., McMahon, C., Robinson, P., Schick, R., Schwarz, L., Simmons, S., Thomas, L., Tyack, P., & Harwood, J. (2014). Using short-term measures of behaviour to estimate long-term fitness of southern elephant seals. Marine Ecology Progress Series496, 99–108. https://doi.org/10.3354/meps10547
3, 6 Committee on the Assessment of the Cumulative Effects of Anthropogenic Stressors on Marine Mammals, Ocean Studies Board, Division on Earth and Life Studies, & National Academies of Sciences, Engineering, and Medicine. (2017). Approaches to Understanding the Cumulative Effects of Stressors on Marine Mammals (p. 23479). National Academies Press. https://doi.org/10.17226/23479
4, 7, 20 Pirotta, E., Booth, C. G., Costa, D. P., Fleishman, E., Kraus, S. D., Lusseau, D., Moretti, D., New, L. F., Schick, R. S., Schwarz, L. K., Simmons, S. E., Thomas, L., Tyack, P. L., Weise, M. J., Wells, R. S., & Harwood, J. (2018). Understanding the population consequences of disturbance. Ecology and Evolution8(19), 9934–9946. https://doi.org/10.1002/ece3.4458
5 Booth, C. G., Sinclair, R. R., & Harwood, J. (2020). Methods for Monitoring for the Population Consequences of Disturbance in Marine Mammals: A Review. Frontiers in Marine Science7, 115. https://doi.org/10.3389/fmars.2020.00115
9, 18 Costa, D. P., Schwarz, L., Robinson, P., Schick, R. S., Morris, P. A., Condit, R., Crocker, D. E., & Kilpatrick, A. M. (2016). A Bioenergetics Approach to Understanding the Population Consequences of Disturbance: Elephant Seals as a Model System. In A. N. Popper & A. Hawkins (Eds.), The Effects of Noise on Aquatic Life II (Vol. 875, pp. 161–169). Springer New York. https://doi.org/10.1007/978-1-4939-2981-8_19
10 New, L. F., Harwood, J., Thomas, L., Donovan, C., Clark, J. S., Hastie, G., Thompson, P. M., Cheney, B., Scott‐Hayward, L., & Lusseau, D. (2013). Modelling the biological significance of behavioural change in coastal bottlenose dolphins in response to disturbance. Functional Ecology27(2), 314–322. https://doi.org/10.1111/1365-2435.12052
11 Pirotta, E., Harwood, J., Thompson, P. M., New, L., Cheney, B., Arso, M., Hammond, P. S., Donovan, C., & Lusseau, D. (2015). Predicting the effects of human developments on individual dolphins to understand potential long-term population consequences. Proceedings of the Royal Society B: Biological Sciences282(1818), 20152109. https://doi.org/10.1098/rspb.2015.2109
12 Reed, J., Harcourt, R., New, L., & Bilgmann, K. (2020). Extreme Effects of Extreme Disturbances: A Simulation Approach to Assess Population Specific Responses. Frontiers in Marine Science7, 519845. https://doi.org/10.3389/fmars.2020.519845
13 Schick, R. S., Kraus, S. D., Rolland, R. M., Knowlton, A. R., Hamilton, P. K., Pettis, H. M., Kenney, R. D., & Clark, J. S. (2013). Using Hierarchical Bayes to Understand Movement, Health, and Survival in the Endangered North Atlantic Right Whale. PLoS ONE8(6), e64166. https://doi.org/10.1371/journal.pone.0064166
14 Rolland, R., Schick, R., Pettis, H., Knowlton, A., Hamilton, P., Clark, J., & Kraus, S. (2016). Health of North Atlantic right whales Eubalaena glacialis over three decades: From individual health to demographic and population health trends. Marine Ecology Progress Series542, 265–282. https://doi.org/10.3354/meps11547
15 Dunlop, R. A., Braithwaite, J., Mortensen, L. O., & Harris, C. M. (2021). Assessing Population-Level Effects of Anthropogenic Disturbance on a Marine Mammal Population. Frontiers in Marine Science8, 624981. https://doi.org/10.3389/fmars.2021.624981
16 Pirotta, E., Mangel, M., Costa, D. P., Goldbogen, J., Harwood, J., Hin, V., Irvine, L. M., Mate, B. R., McHuron, E. A., Palacios, D. M., Schwarz, L. K., & New, L. (2019). Anthropogenic disturbance in a changing environment: Modelling lifetime reproductive success to predict the consequences of multiple stressors on a migratory population. Oikos128(9), 1340–1357. https://doi.org/10.1111/oik.06146
17 Pirotta, E., Booth, C. G., Cade, D. E., Calambokidis, J., Costa, D. P., Fahlbusch, J. A., Friedlaender, A. S., Goldbogen, J. A., Harwood, J., Hazen, E. L., New, L., & Southall, B. L. (2021). Context-dependent variability in the predicted daily energetic costs of disturbance for blue whales. Conservation Physiology9(1), coaa137. https://doi.org/10.1093/conphys/coaa137
19 Harding, H. R., Gordon, T. A. C., Eastcott, E., Simpson, S. D., & Radford, A. N. (2019). Causes and consequences of intraspecific variation in animal responses to anthropogenic noise. Behavioral Ecology30(6), 1501–1511. https://doi.org/10.1093/beheco/arz114