Consistent changes in muscle metabolism underlie dive performance across multiple lineages of diving ducks

Schell, Elizabeth R.; McCracken, Kevin G.; Scott, Graham R.; White, Jeff; Lavretsky, Philip; Dawson, Neal J.

doi:10.1098/rspb.2023.1466

Cited by 3 publications

(1 citation statement)

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“…A breath‐hold is an apnoea either at end‐inspiration, in amphibians and reptiles and also diving birds (Schell et al., 2023 ), cetaceans and sea lions (Ponganis, 2011 ), or following expiration, as in seals (Ponganis, 2011 ). Breath‐hold following end expiration is accompanied by airway closure and relaxation of the expiratory muscles.…”

Section: Commonly Used Scientific Terminology Associated With Intermi...mentioning

confidence: 99%

Breathing patterns and associated cardiovascular changes in intermittently breathing animals: (Partially) correcting a semantic quagmire

Burggren,

Fahlman,

Milsom

2024

Experimental Physiology

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Many animal species do not breathe in a continuous, rhythmic fashion, but rather display a variety of breathing patterns characterized by prolonged periods between breaths (inter‐breath intervals), during which the heart continues to beat. Examples of intermittent breathing abound across the animal kingdom, from crustaceans to cetaceans. With respect to human physiology, intermittent breathing—also termed ‘periodic’ or ‘episodic’ breathing—is associated with a variety of pathologies. Cardiovascular phenomena associated with intermittent breathing in diving species have been termed ‘diving bradycardia’, ‘submersion bradycardia’, ‘immersion bradycardia’, ‘ventilation tachycardia’, ‘respiratory sinus arrhythmia’ and so forth. An examination across the literature of terminology applied to these physiological phenomena indicates, unfortunately, no attempt at standardization. This might be viewed as an esoteric semantic problem except for the fact that many of the terms variously used by different authors carry with them implicit or explicit suggestions of underlying physiological mechanisms and even human‐associated pathologies. In this article, we review several phenomena associated with diving and intermittent breathing, indicate the semantic issues arising from the use of each term, and make recommendations for best practice when applying specific terms to particular cardiorespiratory patterns. Ultimately, we emphasize that the biology—not the semantics—is what is important, but also stress that confusion surrounding underlying mechanisms can be avoided by more careful attention to terms describing physiological changes during intermittent breathing and diving.

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Section: Commonly Used Scientific Terminology Associated With Intermi...mentioning

confidence: 99%

Breathing patterns and associated cardiovascular changes in intermittently breathing animals: (Partially) correcting a semantic quagmire

Burggren,

Fahlman,

Milsom

2024

Experimental Physiology

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Blood‐ and muscle‐O₂ storage capacity in North American diving ducks

Schell,

White,

McCracken

2023

Journal of Avian Biology

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Breath‐hold diving presents air‐breathing vertebrates with the challenge of maintaining aerobic respiration while exercising underwater. Adaptive increases in the oxygen (O2) storage capacity in the lungs, blood, or muscle tissues can enhance these reserves and greatly extend aerobic foraging time underwater. Here, we report blood‐ and muscle‐O2 storage parameters (blood hemoglobin concentration ([Hb]), hematocrit, and myoglobin concentration ([Mb]) in the pectoralis and gastrocnemius) for 16 species of diving and dabbling ducks found in North America, and investigate which parameters are correlated with the diving behaviors reported in both the sea ducks (Mergini) and the pochards (Aythini). Both [Hb] in the blood and [Mb] in the gastrocnemius, a major leg muscle used in propulsion for these predominantly leg‐propelled divers, were significantly higher in the sea ducks compared to the dabblers (Anatini). The pochards also showed a significant increase in [Hb] and were intermediate between the sea ducks and the dabblers in hematocrit and [Mb] in the gastrocnemius. Among these four variables and total body mass, [Mb] in the gastrocnemius was the most significant predictor of mean species dive time, and these two variables were correlated across the phylogeny. Our results indicate that the observed changes in O2 storage capacity in the blood and muscles are positively correlated with diving behavior in two clades of ducks, such that larger increases are correlated with longer dive times.

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Consistent changes in muscle phenotype and mitochondrial abundance underlie dive performance across multiple lineages of diving ducks

Schell,

Scott,

Dawson

et al. 2024

Journal of Experimental Biology

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Diving animals must sustain high muscle activity with finite oxygen (O2) to forage underwater. Studies have shown that some diving mammals exhibit changes in the metabolic phenotype of locomotory muscles compared to non-divers, but the pervasiveness of such changes across diving animals is unclear, particularly among diving birds. Here, we examine whether changes in muscle phenotype and mitochondrial abundance are associated with dive capacity across 17 species of ducks from three distinct evolutionary clades (tribes) in the subfamily Anatinae – the longest diving sea ducks, the mid-tier diving pochards, and the non-diving dabblers. In the gastrocnemius (the primary swimming and diving muscle), mitochondrial volume density in both oxidative and glycolytic fiber types were 70% and 30% higher in sea ducks compared to dabblers, respectively. These differences were associated with preferential proliferation of the subsarcolemmal subfraction, the mitochondria adjacent to the cell membrane and nearest to capillaries, relative to the intermyofibrillar subfraction. Capillary density and capillary-to-fiber ratio were positively correlated with mitochondrial volume density, with no variation in the density of oxidative fiber types across tribes. In the pectoralis, sea ducks had greater abundance of oxidative fiber types than dabblers, whereas pochards were intermediate between the two. These data suggest that skeletal muscles of sea ducks have a heightened capacity for aerobic metabolism and an enhanced ability to utilize O2 stores in the blood and muscle while diving.

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Consistent changes in muscle metabolism underlie dive performance across multiple lineages of diving ducks

Cited by 3 publications

References 63 publications

Breathing patterns and associated cardiovascular changes in intermittently breathing animals: (Partially) correcting a semantic quagmire

Breathing patterns and associated cardiovascular changes in intermittently breathing animals: (Partially) correcting a semantic quagmire

Blood‐ and muscle‐O₂ storage capacity in North American diving ducks

Consistent changes in muscle phenotype and mitochondrial abundance underlie dive performance across multiple lineages of diving ducks

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Consistent changes in muscle metabolism underlie dive performance across multiple lineages of diving ducks

Cited by 3 publications

References 63 publications

Breathing patterns and associated cardiovascular changes in intermittently breathing animals: (Partially) correcting a semantic quagmire

Breathing patterns and associated cardiovascular changes in intermittently breathing animals: (Partially) correcting a semantic quagmire

Blood‐ and muscle‐O2 storage capacity in North American diving ducks

Consistent changes in muscle phenotype and mitochondrial abundance underlie dive performance across multiple lineages of diving ducks

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Product

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Blood‐ and muscle‐O₂ storage capacity in North American diving ducks