Incubation increases oxidative imbalance compared to chick rearing in a seabird, the Magellanic penguin (Spheniscus magellanicus)

Colominas-Ciuró, Roger; Bertellotti, Marcelo; Carabajal, Eliana; D'amico, Veronica Laura; Barbosa, Andrés

doi:10.1007/s00227-017-3139-4

Cited by 7 publications

(6 citation statements)

References 64 publications

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“…Although surprising, given the initial expectations supported by relevant literature (Fletcher et al 2013), similar changes in ROS level throughout the breeding season has been reported in some other species, e.g. in the brown booby Sula leucogaster (Montoya et al 2016), and the Magellanic penguin Spheniscus magellanicus (Colominas-Ciuró et al 2017). Apparently, costs of an increased reproductive effort are not always detected in OS level (Metcalfe and Monaghan 2013, Speakman and Garratt 2014, Costantini 2014.…”

Section: Discussionmentioning

confidence: 61%

Breeding phased dependent oxidative balance in a small High Arctic seabird, the little auk

Kulaszewicz

Wojczulanis‐Jakubas

Jakubas

2018

Journal of Avian Biology

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Reproduction is a demanding phase of bird's life cycle and imposes various physiological challenges. Increasing oxidative stress (OS) has been proposed as one of the costs associated with reproduction. In this study, we investigate the level of OS in a small Arctic seabird, the little auk Alle alle in relation to sex and phase of breeding (incubation, chick‐rearing). We also examine whether OS is related to the birds leucocyte profile. We expected increase in OS with the progress of breeding period (due to increasing energetic demands) and higher values in females (due to high initial investments in production of a large egg). Surprisingly, we found higher OS during incubation compared to chick‐rearing period, suggesting that incubation is a highly demanding reproductive phase in terms of oxidative balance. We suggests that those changes may be attributed to changes in hormone levels affecting oxidative status. Also, in contrasts to our expectations, we did not find sex differences in OS throughout the studied periods of breeding. Finally, we found positive relationships between OS level and haematological parameters: heterophils/lymphocytes ratio, number of leucocytes and lymphocytes per 10 000 erythrocytes, suggesting the effect of the oxidative stress on the immunological system.

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Section: Discussionmentioning

confidence: 61%

Breeding phased dependent oxidative balance in a small High Arctic seabird, the little auk

Kulaszewicz

Wojczulanis‐Jakubas

Jakubas

2018

Journal of Avian Biology

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“…The lack of change in relative mRNA abundance of the other HSPs and REs or in MDA levels during lactation, despite radical changes in body mass and axial girth, is similar to the maintenance of oxidative status during fasting in other capital breeders (Colominas-Ciuró et al 2017 ), including female elephant seals (Sharick et al 2015 ) and may indicate grey seal mothers do not experience increasing blubber oxidative or proteotoxic stress over the lactation fast. Hsc70 , Hsp90 , GPx , CAT and GST explained the majority of the variation in the mRNA abundance data in maternal blubber and could therefore be considered useful transcript-level cellular defence markers during lactation.…”

Section: Discussionmentioning

confidence: 64%

“…Although females of some species have greater cellular defences to protect against oxidative stress during reproduction (Viña et al 2006 ; Borras et al 2007 ), including lactation (Pichaud et al 2013 ), buffering against oxidative damage is not always possible in all tissues (Bergeron et al 2011 ; Zhao et al 2015 ; Stier et al 2017 ; Perrault and Stacy 2018 ) and elevated costs cannot always be matched by increased food intake, resulting in resource limitation and trade-offs in investment in defences. Starvation or fasting itself can be a pro-oxidant state (Sorensen et al 2006 ; Salin et al 2018 ), even in fast-adapted species (Sharick et al 2015 ; Schull et al 2016 ; Colominas-Ciuró et al 2017 ), and can increase HSP levels or expression (Ehrenfried et al 1996 ; Heydari et al 1996 ). Fasting during lactation may thus be particularly challenging due to increased oxidant production when resources are limited.…”

Section: Introductionmentioning

confidence: 99%

“…Conversely, fasting can increase cellular protection and reduce oxidative stress (Longo and Mattson 2014 ; Ensminger et al 2021 ). Fast-adapted species may also buffer oxidant production very effectively (Colominas-Ciuró et al 2017 ; Stier et al 2019 ; Ensminger et al 2021 ). For example, elephant seal pups increase cellular defences and thus avoid oxidative stress in some tissues during fasting (Vázquez-Medina et al 2010 , 2011 ; Martinez et al 2018 ).…”

Section: Introductionmentioning

confidence: 99%

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Fitness correlates of blubber oxidative stress and cellular defences in grey seals (Halichoerus grypus): support for the life-history-oxidative stress theory from an animal model of simultaneous lactation and fasting

Armstrong

Russell

Moss

et al. 2023

Cell Stress and Chaperones

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Life-history-oxidative stress theory predicts that elevated energy costs during reproduction reduce allocation to defences and increase cellular stress, with fitness consequences, particularly when resources are limited. As capital breeders, grey seals are a natural system in which to test this theory. We investigated oxidative damage (malondialdehyde (MDA) concentration) and cellular defences (relative mRNA abundance of heat shock proteins (Hsps) and redox enzymes (REs)) in blubber of wild female grey seals during the lactation fast (n = 17) and summer foraging (n = 13). Transcript abundance of Hsc70 increased, and Nox4, a pro-oxidant enzyme, decreased throughout lactation. Foraging females had higher mRNA abundance of some Hsps and lower RE transcript abundance and MDA concentrations, suggesting they experienced lower oxidative stress than lactating mothers, which diverted resources into pup rearing at the expense of blubber tissue damage. Lactation duration and maternal mass loss rate were both positively related to pup weaning mass. Pups whose mothers had higher blubber glutathione-S-transferase (GST) expression at early lactation gained mass more slowly. Higher glutathione peroxidase (GPx) and lower catalase (CAT) were associated with longer lactation but reduced maternal transfer efficiency and lower pup weaning mass. Cellular stress, and the ability to mount effective cellular defences, could proscribe lactation strategy in grey seal mothers and thus affect pup survival probability. These data support the life-history-oxidative stress hypothesis in a capital breeding mammal and suggest lactation is a period of heightened vulnerability to environmental factors that exacerbate cellular stress. Fitness consequences of stress may thus be accentuated during periods of rapid environmental change.

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“…However, to date, only a few comparative studies have been conducted. Indeed, the results of these studies suggest that incubation is a more demanding phase of reproduction in terms of oxidative balance than chick rearing (Colominas-Ciur o et al 2017a, Kulaszewicz et al 2018, although molt as an energetic life stage was not examined.…”

mentioning

confidence: 99%

Oxidative status and stress during highly energetic life‐history stages of Chinstrap Penguins: breeding versus molting

et al. 2019

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Life‐history stages such as reproduction and molt are energetically costly. Reproductive costs include those associated not only with offspring production, but also protecting and provisioning young. Costs typically associated with molting include decreased thermoregulatory and locomotive performance, and increased metabolic and nutritional costs. Energetic demands may disrupt homeostasis, particularly in terms of its maintenance (e.g., oxidative stress and immunity). Few investigators have explored the relationship between effort (increased metabolic rate) and oxidative status and stress by comparing life‐history stages with different energetic demands. However, comparative studies are crucial for understanding the processes of energy allocation and their consequences for different physiological functions. Our objective was to determine how two highly demanding life‐history stages, breeding and molting, affected oxidative balance in Chinstrap Penguins (Pygoscelis antarcticus), a species where these two activities do not overlap. We found that the heterophil/lymphocyte (H/L) ratio was significantly higher during breeding than molting; oxidative damage was also higher during breeding. In contrast, we found no significant differences between these stages in total antioxidant capacity. We also found sex differences, with males having greater oxidative damage than females. Our results suggest that breeding is more stressful and more demanding for Chinstrap Penguins than molting, and provide further support for the relationship between effort, in terms of increased metabolic rate, and oxidative balance.

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Incubation increases oxidative imbalance compared to chick rearing in a seabird, the Magellanic penguin (Spheniscus magellanicus)

Cited by 7 publications

References 64 publications

Breeding phased dependent oxidative balance in a small High Arctic seabird, the little auk

Breeding phased dependent oxidative balance in a small High Arctic seabird, the little auk

Fitness correlates of blubber oxidative stress and cellular defences in grey seals (Halichoerus grypus): support for the life-history-oxidative stress theory from an animal model of simultaneous lactation and fasting

Oxidative status and stress during highly energetic life‐history stages of Chinstrap Penguins: breeding versus molting

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