Oxidative stress associated with paternal care in smallmouth bass (Micropterus dolomieu)

Wilson, Samantha M.; Gravel, Marie-Ange; Mackie, Trisha A.; Willmore, William G.; Cooke, Steven J.

doi:10.1016/j.cbpa.2012.02.023

Cited by 29 publications

(34 citation statements)

References 63 publications

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“…2011; Wilson et al. 2012; Marri and Richner 2014). Laboratory studies that manipulate oxidative challenge or life‐history investment are pivotal to our ability to establish whether OS may underpin life‐history variation (Metcalfe and Monaghan 2013), and there is emerging experimental evidence that supports this overarching hypothesis (Sohal et al.…”

Section: Introductionmentioning

confidence: 99%

Plasma markers of oxidative stress are uncorrelated in a wild mammal

Christensen

Selman

Blount

et al. 2015

Ecology and Evolution

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Oxidative stress, which results from an imbalance between the production of potentially damaging reactive oxygen species versus antioxidant defenses and repair mechanisms, has been proposed as an important mediator of life‐history trade‐offs. A plethora of biomarkers associated with oxidative stress exist, but few ecological studies have examined the relationships among different markers in organisms experiencing natural conditions or tested whether those relationships are stable across different environments and demographic groups. It is therefore not clear to what extent studies of different markers can be compared, or whether studies that focus on a single marker can draw general conclusions regarding oxidative stress. We measured widely used markers of oxidative damage (protein carbonyls and malondialdehyde) and antioxidant defense (superoxide dismutase and total antioxidant capacity) from 706 plasma samples collected over a 4‐year period in a wild population of Soay sheep on St Kilda. We quantified the correlation structure among these four markers across the entire sample set and also within separate years, age groups (lambs and adults), and sexes. We found some moderately strong correlations between some pairs of markers when data from all 4 years were pooled. However, these correlations were caused by considerable among‐year variation in mean marker values; correlation coefficients were small and not significantly different from zero after accounting for among‐year variation. Furthermore, within each year, age, and sex subgroup, the pairwise correlation coefficients among the four markers were weak, nonsignificant, and distributed around zero. In addition, principal component analysis confirmed that the four markers represented four independent axes of variation. Our results suggest that plasma markers of oxidative stress may vary dramatically among years, presumably due to environmental conditions, and that this variation can induce population‐level correlations among markers even in the absence of any correlations within contemporaneous subgroups. The absence of any consistent correlations within years or demographic subgroups implies that care must be taken when generalizing from observed relationships with oxidative stress markers, as each marker may reflect different and potentially uncoupled biochemical processes.

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Section: Introductionmentioning

confidence: 99%

Plasma markers of oxidative stress are uncorrelated in a wild mammal

Christensen

Selman

Blount

et al. 2015

Ecology and Evolution

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“…at the beginning of the parental care period; males found on eggs <24 h old). Because a recent study in smallmouth bass suggested that oxidative stress does not increase throughout the parental care period (Wilson et al, 2012), it could be reasoned that oxidative stress is not an influencing factor on the life-history tradeoff decision of male smallmouth bass to either stay with or to abandon their brood. The relationship between oxidative stress and reproduction, however, is complex and often indirect and context dependent (Metcalfe and Monaghan, 2013).…”

Section: Discussionmentioning

confidence: 99%

“…If we had used a lethal sampling approach to obtain tissues such as heart, brain or liver, we would have removed the majority of nesting bass for a given year, which would have serious ecological consequences. Previous studies have used plasma for the assessment of oxidative protection and damage (reviewed in Birnie-Gauvin et al, 2017), including research on nesting bass (see Wilson et al, 2012). In addition, other studies on teleost fish have compared different tissues and revealed that plasma concentrations are related to those in other tissues (Taylor et al, 2015).…”

Section: Materials and Methods Study Site Study Animals And Samplingmentioning

confidence: 99%

“…This trade-off is particularly relevant for animals that provide parental care, given their potential requirement for high investments of energy and resources during reproduction (Trivers, 1972). Recently, the association of oxidative stress with reproduction has been investigated in a number of organisms, including the house mouse (Mus musculus domesticus; Garratt et al, 2011), the zebra finch (Taeniopygia guttata; Alonso- and the smallmouth bass (Micropterus dolomieu; Wilson et al, 2012). The relationship between oxidative stress and reproduction is complex and context dependent and, depending on the species and environmental conditions, oxidative stress may have either a stimulatory or inhibitory effect on reproduction.…”

Section: Introductionmentioning

confidence: 99%

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Oxidative ecology of paternal care in wild smallmouth bass, Micropterus dolomieu

Elmer

O’Connor

Philipp

et al. 2017

Journal of Experimental Biology

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Physiologically, oxidative stress is considered a homeostatic imbalance between reactive oxygen species production and absorption. From an ecological perspective, oxidative stress may serve as an important constraint to life-history traits, such as lifespan, reproduction and the immune system, and is gaining interest as a potential mechanism underlying life-history trade-offs. Of late, there has been much interest in understanding the role of oxidative stress in the ecology of wild animals, particularly during challenging periods such as reproduction. Here, we used a long-term study population of a fish with sole-male parental care, the smallmouth bass, Micropterus dolomieu, to examine the associations among oxidative stress indicators and life-history variables in nest-guarding males. In addition, we investigated the potential role of oxidative stress as a physiological mediator of the life-history trade-off decision of paternal smallmouth bass to stay with or abandon their brood. We found that oxidative stress was significantly related to the life history of paternal smallmouth bass, such that older, larger fish with greater reproductive experience and larger broods nesting in cooler water temperatures had lower levels of oxidative stress. However, we found no significant correlation between oxidative stress and nesting success, suggesting that oxidative stress may not be involved in the decision of male smallmouth bass to abandon their brood. Wild fish have been relatively understudied in the emerging field of oxidative ecology, and this study makes noteworthy contributions by revealing interesting connections between the life histories of paternal smallmouth bass and their oxidative status.

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“…Studies in the field, however, have been exclusively restricted to analyses of a single tissue (blood) [see the above references for mammals; Speakman and Garratt (2013) for references to seven species of birds; Isaksson, While, Olsson, Komdeur, and Wapstra (2011) and Wilson, Gravel, Mackie, Willmore, and Cooke (2012) for reptiles and the fish]. It is therefore unclear whether the diversity in tissue response is an artifact of studying animals in captivity with ad libitum access to food that is generally also supplemented with large amounts of exogenous antioxidants.…”

Section: Introductionmentioning

confidence: 99%

Oxidative damage and antioxidant defense are assay and tissue‐dependent both in captive and wild‐caught bank voles (Myodes glareolus) before and after reproduction

Ołdakowski

Taylor

2018

Ecology and Evolution

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Reproduction is costly and life‐history theory predicts that current parental investment will result in lower survival or decreased future reproduction. The physiological mechanisms mediating the link between reproduction and survival are still under debate and elevated oxidative damage during reproduction has been proposed as a plausible candidate. Previous studies of oxidative stress during reproduction in animals under natural conditions have been restricted to analyses of blood. Herein, we measured the level of oxidative damage to lipids (tiobarbituric‐acid‐reactive substances) and proteins (carbonyls) in the liver, kidneys, heart and skeletal muscles in free‐living bank vole females from spring and autumn generations, before and after reproduction. Antioxidant defense in the liver and kidneys was also determined. We expected oxidative damage to tissues and hypothesized that the damage would be more uniform between tissues in wild animals compared to those breeding under laboratory conditions. Considering all combinations of markers/tissues/generations, oxidative damage in females did not differ before and after reproduction in 12 comparisons, was lower after reproduction in three comparisons, and was higher after breeding in one comparison. The total glutathione was significantly increased after reproduction only in the liver of the autumn generation and there was no change in catalase activity. Our results confirm—for the first time in the field—previous observations from laboratory studies that there is no simple link between oxidative stress and reproduction and that patterns depend on the tissue and marker being studied. Overall, however, our study does not support the hypothesis that the cost of reproduction in bank voles is mediated by oxidative stress in these tissues.

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Oxidative stress associated with paternal care in smallmouth bass (Micropterus dolomieu)

Cited by 29 publications

References 63 publications

Plasma markers of oxidative stress are uncorrelated in a wild mammal

Plasma markers of oxidative stress are uncorrelated in a wild mammal

Oxidative ecology of paternal care in wild smallmouth bass, Micropterus dolomieu

Oxidative damage and antioxidant defense are assay and tissue‐dependent both in captive and wild‐caught bank voles (Myodes glareolus) before and after reproduction

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