The challenges of maintaining oxidative balance for migratory
birds
During energetically-challenging periods, all aerobic organisms must
contend with an increased production of reactive species (RS) by either
neutralizing the RS with antioxidants to minimize resulting oxidative
damage, or damage must be restored using repair mechanisms (Halliwell
and Gutteridge 2007, Costantini 2014, 2019). Long-distance flight
increases metabolism (Swanson 2010, Corder and Schaeffer 2015,
DeMoranville et al. 2019, Bishop, C.M., Guglielmo 2022) and poses a
potential oxidative challenge for flying animals (McWilliams et al.
2021, McWilliams, S.R., Ramenofsky, M., Pierce 2022). For example,
Nathusius’ bats Pipistrellus nathusii that were captured and
sampled during a migratory flight had higher circulating oxidative
damage markers compared to individuals that were captured and rested for
18-24 hours (Costantini et al. 2018). Similarly, circulating protein
damage and the antioxidant enzyme glutathione peroxidase (GPx) were
higher in European robins Erithacus rubecula during a nocturnal
migratory flight compared to resting individuals caught during the day,
indicating that damage to muscle occurs with flight and the antioxidant
system can respond rapidly (Jenni-Eiermann et al. 2014). These acute
effects of flight were also demonstrated in captive Yellow-rumped
warblers (Setophaga coronata coronate) , as protein carbonyls and
superoxide dismutase (SOD) activity were higher in the pectoralis muscle
immediately after a flight in a wind tunnel compared to individuals at
rest (Dick and Guglielmo 2019). Similarly, flight-trained zebra finchesTaeniopygia guttata had increased circulating oxidative damage
compared to untrained sedentary individuals (Skrip et al. 2016). These
studies together demonstrate that migratory bats and birds respond to
such oxidative challenges by increasing antioxidant enzyme activities,
depleting or augmenting non-enzymatic antioxidant capacity, and in these
cases increasing oxidative damage. They also reveal that too little is
known about tissue-specific oxidative status of migratory birds (Dick
and Guglielmo 2019) and the extent to which an individual’s circulating
oxidative status reflects the oxidative state of muscles and organs at a
given time (Costantini 2019, Frawley et al. 2021a). What remains to be
determined for migratory songbirds is how the oxidative status of
different tissues and plasma responds to both flight training and
ecologically-relevant differences in diet quality (i.e. antioxidants and
fat composition).
Certain dietary fats challenge the antioxidant system - Birds rely
primarily on fatty acids to fuel flight (Guglielmo, 2018; McWilliams,
Guglielmo, Pierce, & Klaassen, 2004), and several species of migratory
songbirds increase the amounts of unsaturated fats and especially
long-chain polyunsaturated fats (PUFAs) in their diet, fat stores and in
circulation during migration compared to non-migration periods (Pierce
et al. 2004, Pierce and McWilliams 2005, Price et al. 2008, Smith and
McWilliams 2010, Jensen et al. 2020, McWilliams, S.R., Ramenofsky, M.,
Pierce 2022). The potential benefits of consuming certain long-chain
PUFA (e.g., 18:2n-6 PUFA) including enhanced efficiency of energy
metabolism during exercise and reduced flight costs (Pierce and
McWilliams 2014, Guglielmo 2018), are also associated with potential
oxidative costs because PUFA are highly susceptible to oxidative damage
(Halliwell and Gutteridge 2007, Skrip and McWilliams 2016, McWilliams et
al. 2020). The resulting lipid radicals often cause a self-perpetuating
chain reaction damaging nearby PUFAs and other molecules (Halliwell and
Gutteridge 2007, Skrip and McWilliams 2016, Cooper-Mullin et al. 2019).
Birds preferentially consuming 18:2n-6 PUFA during migration to enhance
their metabolism (Pierce and McWilliams 2014) likely require an
augmented antioxidant system to protect against the oxidative challenge
that such PUFAs pose (McWilliams et al. 2021).
Dietary antioxidants augment the antioxidant system - Many
songbird species select fruits that are high in antioxidants and fat
during fall (post-breeding) migration, suggesting that antioxidant
consumption may be important to protect against oxidative damage during
this life history stage (Alan and McWilliams 2013, Bolser et al. 2013).
Water-soluble antioxidants such as anthocyanins are preferentially
consumed by certain songbird species during fall migration and in
cafeteria-style choice experiments (Schaefer et al. 2008, Alan et al.
2013, Bolser et al. 2013). Anthocyanins are potent antioxidants
(Halliwell and Gutteridge 2007) that are exclusively stable at acidic pH
levels (i.e. they degrade extensively in less than an hour at pH 7.4)
and are more likely to remain intact and absorbed in the 2 orders of
magnitude more acidic stomachs of songbirds (pH 2) relative to mammals
(pH 4.4) (Dangles and Fenger 2018). Anthocyanins can directly or
indirectly affect the antioxidant system and also have been shown to
protect birds from an immune challenge (Catoni et al. 2008) and protect
against some of the metabolic costs associated with flight training
(Casagrande et al. 2020) as well as courtship (Carbeck et al. 2018) and
reproduction in spring (Frawley et al. 2021b). These energy savings
associated with consuming anthocyanins may allow birds to invest in
increasing enzymatic or non-enzymatic antioxidants to prevent damage
(McWilliams et al. 2020). Non-enzymatic antioxidant capacity increases
with fat stores in songbirds on stopovers during migration (Costantini
et al. 2007, Skrip et al. 2015) and is greatest during the pre-migratory
fueling stage in shorebirds (Gutiérrez et al. 2019). Thus, hyperphagia
associated with preparation for migration in birds may augment their
antioxidant system by increasing fat-soluble antioxidants stored within
newly accumulated fat stores or by increasing water-soluble antioxidant
metabolites continuously released by gut microbes (Dogan Comert and
Gokman 2017).