Links between energy budgets, somatic condition, and life history reveal heterogeneous energy management tactics in a group-living mesocarnivore
Abstract Background Optimal management of voluntary energy expenditure is crucial to the survival and reproductive success of wild animals. Nevertheless, a growing appreciation of inter-individual variation in the internal state driving movement suggests that individuals may follow different, yet eq...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2024-03-01
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| Series: | Movement Ecology |
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| Online Access: | https://doi.org/10.1186/s40462-024-00453-1 |
| _version_ | 1827300868418961408 |
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| author | Julius G. Bright Ross Andrew Markham Christina D. Buesching Catherine Hambly John R. Speakman David W. Macdonald Chris Newman |
| author_facet | Julius G. Bright Ross Andrew Markham Christina D. Buesching Catherine Hambly John R. Speakman David W. Macdonald Chris Newman |
| author_sort | Julius G. Bright Ross |
| collection | DOAJ |
| description | Abstract Background Optimal management of voluntary energy expenditure is crucial to the survival and reproductive success of wild animals. Nevertheless, a growing appreciation of inter-individual variation in the internal state driving movement suggests that individuals may follow different, yet equally optimal tactics under the same environmental conditions. However, few studies in wild populations have investigated the occurrence and demographic context of different contemporaneous energetic expenditure tactics. Here, we explore this neglected aspect of energy budgeting in order to determine the effect of life-history traits such as age and reproductive status on the co-occurrence of different energy-budgeting tactics in wild populations. Methods We investigated inter-individual heterogeneity in energy expenditure within a wild population of European badgers (Meles meles) by quantifying individual overall dynamic body acceleration (ODBA, from tri-axial accelerometry collars) and total daily energy expenditure (DEE, from doubly-labelled water) during 6–9 day deployments and dosing periods over six different seasons (spring, summer, and autumn) in 2018–2019. We obtained ODBA values for 41 deployments (24 unique badgers) and DEE measurements for 41 dosings (22 unique badgers). We then evaluated correlations between these energetic metrics and computed individual ratios of ODBA/DEE as a proxy for the proportion of total energy spent on activity. We measured the impact of alternative ODBA/DEE ratios on body condition, and use survival models constructed using 29 years of demographic data from the same population to situate body-condition changes in the context of age and reproductive status. Results Both ODBA and DEE were highly variable between individuals and exhibited season-specific relationships with individual body condition and life-history factors. DEE scaled allometrically with body weight, but only in summer and autumn; post-reproductive female badgers were lighter than other badgers during the spring but expended on average 350 kJ/day more than predicted from allometric scaling. Older badgers expended significantly less energy on movement during the summer than did younger adults. The ratio of ODBA to DEE (OD) provides a measure of proportional investment into movement. This ratio correlated more significantly with next-season body condition than either energetic metric did independently. However, the majority of individuals with high OD ratios were either younger badgers or reproductive females, for which lower body condition typically presented less of a mortality risk in previous analyses of this population. Conclusions Within a single population under the same environmental conditions, we found wide inter-individual variation in both mechanical and total energy expenditure. The adoption of different tactics aligns with relationships between life-history parameters and mortality risk previously studied within the population. Crucially, younger badgers and reproductive females appeared able to tolerate energy expenditure tactics that depleted their body condition more than other badgers. These findings provide a mechanism by which differences in individual energetic context set by life history can maintain heterogeneity in wild populations, providing a wide range of potential energetic tactics under changing environmental conditions. |
| first_indexed | 2024-04-24T16:12:19Z |
| format | Article |
| id | doaj.art-9393cbd27f594c2e8db79fcdf5769f61 |
| institution | Directory Open Access Journal |
| issn | 2051-3933 |
| language | English |
| last_indexed | 2024-04-24T16:12:19Z |
| publishDate | 2024-03-01 |
| publisher | BMC |
| record_format | Article |
| series | Movement Ecology |
| spelling | doaj.art-9393cbd27f594c2e8db79fcdf5769f612024-03-31T11:38:24ZengBMCMovement Ecology2051-39332024-03-0112111410.1186/s40462-024-00453-1Links between energy budgets, somatic condition, and life history reveal heterogeneous energy management tactics in a group-living mesocarnivoreJulius G. Bright Ross0Andrew Markham1Christina D. Buesching2Catherine Hambly3John R. Speakman4David W. Macdonald5Chris Newman6Wildlife Conservation Research Unit, Department of Biology, The Recanati-Kaplan Centre, University of OxfordDepartment of Computer Science, University of OxfordThe Irving K. Barber School of Arts and Sciences, The University of British ColumbiaInstitute of Biological and Environmental Sciences, University of AberdeenInstitute of Biological and Environmental Sciences, University of AberdeenWildlife Conservation Research Unit, Department of Biology, The Recanati-Kaplan Centre, University of OxfordWildlife Conservation Research Unit, Department of Biology, The Recanati-Kaplan Centre, University of OxfordAbstract Background Optimal management of voluntary energy expenditure is crucial to the survival and reproductive success of wild animals. Nevertheless, a growing appreciation of inter-individual variation in the internal state driving movement suggests that individuals may follow different, yet equally optimal tactics under the same environmental conditions. However, few studies in wild populations have investigated the occurrence and demographic context of different contemporaneous energetic expenditure tactics. Here, we explore this neglected aspect of energy budgeting in order to determine the effect of life-history traits such as age and reproductive status on the co-occurrence of different energy-budgeting tactics in wild populations. Methods We investigated inter-individual heterogeneity in energy expenditure within a wild population of European badgers (Meles meles) by quantifying individual overall dynamic body acceleration (ODBA, from tri-axial accelerometry collars) and total daily energy expenditure (DEE, from doubly-labelled water) during 6–9 day deployments and dosing periods over six different seasons (spring, summer, and autumn) in 2018–2019. We obtained ODBA values for 41 deployments (24 unique badgers) and DEE measurements for 41 dosings (22 unique badgers). We then evaluated correlations between these energetic metrics and computed individual ratios of ODBA/DEE as a proxy for the proportion of total energy spent on activity. We measured the impact of alternative ODBA/DEE ratios on body condition, and use survival models constructed using 29 years of demographic data from the same population to situate body-condition changes in the context of age and reproductive status. Results Both ODBA and DEE were highly variable between individuals and exhibited season-specific relationships with individual body condition and life-history factors. DEE scaled allometrically with body weight, but only in summer and autumn; post-reproductive female badgers were lighter than other badgers during the spring but expended on average 350 kJ/day more than predicted from allometric scaling. Older badgers expended significantly less energy on movement during the summer than did younger adults. The ratio of ODBA to DEE (OD) provides a measure of proportional investment into movement. This ratio correlated more significantly with next-season body condition than either energetic metric did independently. However, the majority of individuals with high OD ratios were either younger badgers or reproductive females, for which lower body condition typically presented less of a mortality risk in previous analyses of this population. Conclusions Within a single population under the same environmental conditions, we found wide inter-individual variation in both mechanical and total energy expenditure. The adoption of different tactics aligns with relationships between life-history parameters and mortality risk previously studied within the population. Crucially, younger badgers and reproductive females appeared able to tolerate energy expenditure tactics that depleted their body condition more than other badgers. These findings provide a mechanism by which differences in individual energetic context set by life history can maintain heterogeneity in wild populations, providing a wide range of potential energetic tactics under changing environmental conditions.https://doi.org/10.1186/s40462-024-00453-1Daily energy expenditureDoubly-labelled waterEnergy budgetingEnergetic ecologyLife-history trade-offsOverall dynamic body acceleration |
| spellingShingle | Julius G. Bright Ross Andrew Markham Christina D. Buesching Catherine Hambly John R. Speakman David W. Macdonald Chris Newman Links between energy budgets, somatic condition, and life history reveal heterogeneous energy management tactics in a group-living mesocarnivore Movement Ecology Daily energy expenditure Doubly-labelled water Energy budgeting Energetic ecology Life-history trade-offs Overall dynamic body acceleration |
| title | Links between energy budgets, somatic condition, and life history reveal heterogeneous energy management tactics in a group-living mesocarnivore |
| title_full | Links between energy budgets, somatic condition, and life history reveal heterogeneous energy management tactics in a group-living mesocarnivore |
| title_fullStr | Links between energy budgets, somatic condition, and life history reveal heterogeneous energy management tactics in a group-living mesocarnivore |
| title_full_unstemmed | Links between energy budgets, somatic condition, and life history reveal heterogeneous energy management tactics in a group-living mesocarnivore |
| title_short | Links between energy budgets, somatic condition, and life history reveal heterogeneous energy management tactics in a group-living mesocarnivore |
| title_sort | links between energy budgets somatic condition and life history reveal heterogeneous energy management tactics in a group living mesocarnivore |
| topic | Daily energy expenditure Doubly-labelled water Energy budgeting Energetic ecology Life-history trade-offs Overall dynamic body acceleration |
| url | https://doi.org/10.1186/s40462-024-00453-1 |
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