Gill morphometrics in relation to gas transfer and ram ventilation in high‐energy demand teleosts: Scombrids and billfishes

Wegner, Nicholas C.; Sepúlveda, Chugey A.; Bull, Kristina B.; Graham, John L.

doi:10.1002/jmor.10777

Cited by 80 publications

(92 citation statements)

References 45 publications

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“…Direct oxygen tolerance measurements for adult billfishes are not available, although one juvenile sailfish (Istiophorus platypterus) study indicated high oxygen consumption and typical metabolic rates associated with tropical tunas 19 . These high-oxygen-demand species also share obligate ram ventilation respiration, large gill surface and intolerance to low ambient dissolved oxygen 15,17,20,21 . Here, we consider the plausible hypothesis that these species have oxygen limitations that impact vertical habitat use.…”

Section: Figure 1 | Blue Marlin M Nigricans With An Electronic Tag Umentioning

confidence: 99%

Expansion of oxygen minimum zones may reduce available habitat for tropical pelagic fishes

et al. 2011

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Habitat compression and associated potential habitat loss was validated using electronic tagging data from 47 blue marlin. This phenomenon increases vulnerability to surface fishing gear for billfishes and tunas 8,9 , and may be associated with a 10-50% worldwide decline of pelagic predator diversity 10 . Further expansion of the Atlantic OMZ along with overfishing may threaten the sustainability of these valuable pelagic fisheries and marine ecosystems.Dissolved oxygen is critical for sustaining most marine animal life. When dissolved oxygen is minimized, widespread mortality 11,12 or avoidance 13 of affected areas can result. OMZs in the eastern tropical seas represent the largest contiguous areas of naturally occurring hypoxia 9 in the world's oceans. In the present climate change cycle, characterized by anthropogenic CO 2 emissions 2 and global warming, these areas are expanding and shoaling 3,12,14 . Possible consequences of OMZ expansion to the marine ecosystem 14 include loss of vertical habitat for high-oxygen-demand tropical pelagic billfishes and tunas and the associated increased risk of overfishing of these species by surface fishing gear 8,9 .Large-scale expansion of OMZs over the past 50 years 3 poses a challenge for predicting impacts to pelagic fish stocks and their ecosystem. Although oceanographic modelling and ocean observations for retrospective analyses are useful for examining past trends, understanding future OMZ expansions and the concurrent impacts on billfish and tuna populations is essential for preventing overfishing. We analysed recent hypoxia data associated with OMZ expansion in the eastern tropical Atlantic (ETA) to examine possible habitat loss of the near-surface layer. We also present vertical habitat use data of Atlantic blue marlin (Makaira nigricans) monitored with electronic tags (Fig. 1). Changes in habitat use were validated by maximum daily depths

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Section: Figure 1 | Blue Marlin M Nigricans With An Electronic Tag Umentioning

confidence: 99%

Expansion of oxygen minimum zones may reduce available habitat for tropical pelagic fishes

et al. 2011

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“…The genera Paratrygon and Plesiotrygon may be included in this group. Several authors agree that gill area is linked to the activity of the fish (Gray, 1954;Wegner et al, 2010). For example, the gill filament number is higher in the faster swimming Atlantic sharpnose Rhizoprionodon terraenovae (Richardson, 1836) than in more benthic smooth dogfish shark Mustelus canis (Mitchill, 1815) (Schwartz et al, 1993).…”

Section: Interspecific Variations Among Potamotrygonid Embryosmentioning

confidence: 99%

“…The gill dimensions can also be influenced by the level of an animal's activity. Both teleosts and elasmobranchs with high metabolic requirements have gill specialisations facilitating gas transfer De Jager & Dekkers, 1975;Wegner et al, 2010). Like teleosts, active pelagic elasmobranchs have a large gill area, densely packed lamellae, and a low water-blood barrier (Hughes & Wright, 1970).…”

Section: Introductionmentioning

confidence: 99%

“…The relationships between gill and body measurements have been investigated for a large number of teleosts, both marine and freshwater species (Karakatsouli et al, 2006;Wegner et al, 2010). To date, such comparisons have only been made for marine elasmobranch species (Emery & Szczepanski, 1986;Hughes et al, 1986), and few studies have been conducted in freshwater elasmobranchs.…”

Section: Introductionmentioning

confidence: 99%

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Gill dimensions in near-term embryos of Amazonian freshwater stingrays (Elasmobranchii: Potamotrygonidae) and their relationship to the lifestyle and habitat of neonatal pups

2015

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This comparative study of gill morphometrics in near-term embryos of freshwater stingray potamotrygonids examines gill dimensions in relation to neonatal lifestyle and habitat. In embryos of the potamotrygonids Paratrygon aiereba, Plesiotrygon iwamae, Potamotrygon motoro, Potamotrygon orbignyi, and cururu ray Potamotrygon sp. the number and length of filaments, total gill surface area, mass-specific surface area, water-blood diffusion distance, and anatomical diffusion factor were analysed. In all potamotrygonids, the 3 rd branchial arch possessed a larger respiratory surface than the other gill arches. Larger embryos had more gill surface area and large spiracles, which are necessary to maintain the high oxygen uptake needed due to their larger body size. However, the higher mass-specific gill surface area observed in near-term embryos may be advantageous because neonates can use hypoxic environments as refuges against predators, as well as catch small prey that inhabit the same environment. As expected from their benthic mode of life, freshwater stingrays are sluggish animals compared to pelagic fishes. However, based on gill respiratory morphometry (such as gill area, mass-specific gill area, the water-blood diffusion barrier, anatomical diffusion factor, and relative opening of the spiracle), subtypes of lifestyles can be observed corresponding to: active, intermediate, and sluggish species according to Gray's scale.Este estudo realizado com embriões a termo de arraias de água doce (Potamotrygonidae) compara e analisa as dimensões branquiais em relação ao estilo de vida e habitat dos neonatos. Nos embriões de Paratrygon aiereba, Plesiotrygon iwamae, Potamotrygon motoro, Potamotrygon orbignyi e Potamotrygon sp. (arraia cururu) foram analisados número e comprimento dos filamentos, área branquial, área superficial branquial massa-específica, barreira de difusão água-sangue e fator de difusão anatômico. Em todos os potamotrigonídeos estudados, o 3º arco branquial possui uma superfície respiratória maior que os demais arcos. Embriões de espécies de maior porte possuem grandes espiráculos e maior área de superfície branquial. Isso ajuda a manter a taxa de absorção de oxigênio proporcional ao requerimento do animal. No entanto, a grande área de superfície branquial massa-específica observadas nos embriões a termo pode ser vantajosa, pois os neonatos podem usar ambientes hipóxicos como refúgios contra predadores, bem como capturar pequenas presas que habitam o mesmo ambiente. Devido ao modo de vida bentônico, as arraias de água doce são nadadoras lentas comparadas aos peixes pelágicos. No entanto, com base na morfometria branquial (área de superfície branquial, área branquial massa-específica, barreira de difusão água-sangue, fator de difusão anatômico e abertura relativa do espiráculo), subtipos de estilos de vida podem ser observados: ativas, intermediárias e lentas, conforme escala definida por Gray.

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“…Most previous studies on the structure of fish gills have focused on the dependence of the total surface area of the gill upon the body size and species of fish (1,4,5). We consider the convective oxygen transfer that occurs in fish gills.…”

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confidence: 99%

Optimal lamellar arrangement in fish gills

Park

Kim

2014

Proc. Natl. Acad. Sci. U.S.A.

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Fish respire through gills, which have evolved to extract aqueous oxygen. Fish gills consist of filaments with well-ordered lamellar structures, which play a role in maximizing oxygen diffusion. It is interesting that when we anatomically observe the gills of various fish species, gill interlamellar distances (d) vary little among them, despite large variations in body mass (M b ). Noting that the small channels formed by densely packed lamellae cause significant viscous resistance to water flow, we construct and test a model of oxygen transfer rate as a function of the lamellar dimensions and pumping pressure, which allows us to predict the optimal interlamellar distance that maximizes the oxygen transfer rate in the gill. Comparing our theory with biological data supports the hypothesis that fish gills have evolved to form the optimal interlamellar distances for maximizing oxygen transfer. This explains the weak scaling dependence offish respiration | biomechanics | biofluiddynamics F ish gills have evolved exclusively in aquatic creatures to extract aqueous oxygen. Because oxygen has considerably low solubility and diffusivity in water, the efficiency of respiration is critical (1). Gills consist of plate-like structures called filaments that are covered by an array of lamellae enclosing a capillary blood network, as shown in Fig. 1 (1, 2). Oxygen-rich water passes through the narrow channels formed by the lamellar layers, where oxygen diffuses into the capillaries. The densely packed lamellar structure is advantageous because it provides a large surface area for oxygen transfer; however, it also generates considerable viscous resistance. This resistance is overcome by pumping. Fish typically adopt one of the following two pumping mechanisms: branchial pumping and ram ventilation. Most teleost fish, members of the diverse group of ray-finned fish, use branchial pumping, and muscular compression in the pharynx enables water flow through the gills. In ram ventilation, which is used by many pelagic fish, the dynamic pressure generated by their swimming drives water flow into the gills (3).Most previous studies on the structure of fish gills have focused on the dependence of the total surface area of the gill upon the body size and species of fish (1, 4, 5). We consider the convective oxygen transfer that occurs in fish gills. As water passes through the narrow lamellar channels, increased viscous resistance impedes water flow at a given pumping pressure, which is limited by muscle power or swimming speeds; this leads to a lowering of the oxygen transfer rate. Hence, the flow rate within the gaps of the lamellae and the extended surface area play important roles in determining the oxygen transfer rate. The number of lamellae per unit length of gill filament determines both the surface area for diffusion and the size of the water channels. Therefore, we investigate the relationship between lamellar distance and oxygen transfer rate, an aspect that previously has seldom been explored. ResultsTheoretical Analysis. W...

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Gill morphometrics in relation to gas transfer and ram ventilation in high‐energy demand teleosts: Scombrids and billfishes

Cited by 80 publications

References 45 publications

Expansion of oxygen minimum zones may reduce available habitat for tropical pelagic fishes

Expansion of oxygen minimum zones may reduce available habitat for tropical pelagic fishes

Gill dimensions in near-term embryos of Amazonian freshwater stingrays (Elasmobranchii: Potamotrygonidae) and their relationship to the lifestyle and habitat of neonatal pups

Optimal lamellar arrangement in fish gills

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