Interactive effects of salinity and temperature acclimation on gill morphology and gene expression in threespine stickleback

Gibbons, Taylor C.; McBryan, Tara L.; Schulte, Patricia M.

doi:10.1016/j.cbpa.2018.03.013

Cited by 26 publications

(13 citation statements)

References 63 publications

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“…Like its close relative the crucian carp, the goldfish (Carassius auratus) was observed to undergo reversible gill remodeling (65), and indeed reversible gill remodeling was detected in all but one of the eleven cyprinid species examined to date (14,37,80). Reversible gill remodeling has also been identified in a catfish (56), an eel (70), a stickleback (21), and one salmonid species (2), as well as a few cyprinodontiform fishes (1,44). Among these fishes are three species found in marine and brackish water, the Atlantic killifish (Fundulus heteroclitus) (1,38), the mangrove rivulus (Kryptolebias marmoratus) (44), and the threespine stickleback (Gasterosteus aculeatus) (21).…”

Section: Reversible Gill Remodeling: a Solution To Constraints On The Design Of Respiratory Systems?mentioning

confidence: 99%

“…Reversible gill remodeling has also been identified in a catfish (56), an eel (70), a stickleback (21), and one salmonid species (2), as well as a few cyprinodontiform fishes (1,44). Among these fishes are three species found in marine and brackish water, the Atlantic killifish (Fundulus heteroclitus) (1,38), the mangrove rivulus (Kryptolebias marmoratus) (44), and the threespine stickleback (Gasterosteus aculeatus) (21). Because they are hypo-osmotic to their environment, marine teleost fish face osmotic water loss and diffusive ion gain across the gill, and they counter these challenges to the maintenance of salt and water balance by drinking sea water and by actively excreting salt via salt-secreting ionocytes in the gill (18,35).…”

Section: Reversible Gill Remodeling: a Solution To Constraints On The Design Of Respiratory Systems?mentioning

confidence: 99%

“…The mechanisms underlying the presumptive shedding of the ILCM have not yet been described and thus form an area of research ripe for future investigation. Investigation is also needed to characterize the signaling mechanisms responsible for reversible gill remodeling in response to cues other than O 2 uptake, including toxicants (62), salinity (2,21,34,57,69), and air exposure (44).…”

Section: Signals and Mechanisms Underlying Gill Remodelingmentioning

confidence: 99%

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Conflict and Compromise: Using Reversible Remodeling to Manage Competing Physiological Demands at the Fish Gill

Gilmour

Perry

2018

Physiology

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The structural features of the fish gill necessary for oxygen uptake also favor undesirable, passive movements of ions and water. Reversible gill remodeling is one solution to this conflict. Cell masses that limit functional surface area are lost when oxygen availability decreases in hypoxia or oxygen demand increases with exercise or high temperature. However, much remains to be learned about how widespread reversible gill remodeling is among fish species, and how and why it occurs.

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Section: Reversible Gill Remodeling: a Solution To Constraints On The Design Of Respiratory Systems?mentioning

confidence: 99%

Section: Reversible Gill Remodeling: a Solution To Constraints On The Design Of Respiratory Systems?mentioning

confidence: 99%

Section: Signals and Mechanisms Underlying Gill Remodelingmentioning

confidence: 99%

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Conflict and Compromise: Using Reversible Remodeling to Manage Competing Physiological Demands at the Fish Gill

Gilmour

Perry

2018

Physiology

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“…These responses may provide structural support for the lamellae, or may limit evaporative water loss across the gills via reduction of functional surface area (Nilsson, Dymowska, & Stecyk, 2012;Wright, 2012). Modification of gill surface area via modulation of an ILCM also occurs in several other groups of fully aquatic teleost fishes, including cyprinids (Dhillon et al, 2013;Sollid, De Angelis, Gundersen, & Nilsson, 2003;Tzaneva, Bailey, & Perry, 2011;Wu et al, 2017), catfishes (Phuong, Huong, Nyengaard, & Bayley, 2017), stickleback (Gibbons, McBryan, & Schulte, 2018), and salmonids (Blair, Matheson, He, & Goss, 2016). In these species, the ILCM is comprised of many cell types, including epithelial cells, mucous cells, ionocytes (mitochondria rich cells), neuroepithelial cells, and undifferentiated cells (Blair, Matheson, & Goss, 2017;Dhillon et al, 2013;Sinha, Matey, Giblen, Blust, & De Boeck, 2014;Sollid, Weber, & Nilsson, 2005).…”

Section: Introductionmentioning

confidence: 99%

Gill remodelling during terrestrial acclimation in the amphibious fish Polypterus senegalus

Turko

Maini

Wright

et al. 2019

Journal of Morphology

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Fishes are effectively weightless in water due to the buoyant support of the environment, but amphibious fishes must cope with increased effective weight when on land. Delicate structures such as gills are especially vulnerable to collapse and loss of surface area out of water. We tested the ‘structural support’ hypothesis that amphibious Polypterus senegalus solve this problem using phenotypically plastic changes that provide mechanical support and increase stiffness at the level of the gill lamellae, the filaments, and the whole arches. After 7 d in terrestrial conditions, enlargement of an inter‐lamellar cell mass filled the water channels between gill lamellae, possibly to provide structural support and/or reduce evaporative water loss. Similar gill remodelling has been described in several other actinopterygian fishes, suggesting this may be an ancestral trait. There was no change in the mechanical properties or collagen composition of filaments or arches after 7 days out of water, but 8 months of terrestrial acclimation caused a reduction in gill arch length and mineralized bone volume. Thus, rather than increasing the size and stiffness of the gill skeleton, P. senegalus may instead reduce investment in supportive gill tissue while on land. These results are strikingly similar to the evolutionary trend of gill loss that occurred during the tetrapod invasion of land, raising the possibility that genetic assimilation of gill plasticity was an underlying mechanism.

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“…Elevated salinity in freshwater habitats spurs a suite of negative effects across biological levels, from genetic to ecosystem (Hintz et al, 2017;Gibbons et al, 2018;Merrick and Searle, 2019;Venâncio et al, 2019). For many freshwater taxa, salt pollution causes numerous sublethal effects, including changes in foraging and anti-predator behavior (Hall et al, 2017); changes in life history traits (Faulkner et al, 2019); and increased malformations (Brady, 2013;Hopkins et al, 2013;Alam et al, 2020).…”

Section: Salt Pollution: a Widespread Problem For Freshwater Organismsmentioning

confidence: 99%

Road salt compromises functional morphology of larval gills in populations of an amphibian

Szeligowski

Scanley

Broadbridge

et al. 2020

Preprint

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Throughout much of the world, winter deicing practices have led to secondary salinization of freshwater habitats, where numerous taxa are vulnerable to elevated salinity. Many amphibians are of particular concern because of their permeable skin and reliance on small ponds and pools, where salinity levels can be high. The early life-history stages of amphibians that develop in these habitats are especially sensitive to salt exposure. Larvae developing in salt-polluted environments must osmoregulate through ion exchange in gills. While salt-induced changes to the physiology of ion exchange in amphibian gills is generally understood, functionally relevant changes in gill morphology remain poorly described. Yet the structure of gills should be an important component affecting their ionoregulatory capacity, for instance in terms available surface area. Larval amphibian gills also play critical roles in gas exchange and foraging. Thus, changes in gill morphology due to salt pollution potentially affect not only osmoregulation, but also respiration and feeding. Here, we used a chronic exposure experiment to quantify the effect of salinity on larval gill morphology in populations of the wood frog (Rana sylvatica). We measured a suite of morphological traits on gill tufts, where ionoregulation and gas exchange occur, and on gill filters, which are used in feeding. Larvae raised in high salinity conditions had gill tufts with lower surface area to volume ratio, while epithelial cells on these tufts were less circular but occurred at higher densities. Gill filters showed increased spacing, which can potentially reduce their efficiency in filtering food particles. Together, these changes seem likely to diminish the ionoregulatory and respiratory capacity of gill tufts, and compromise feeding functionality of gill filters. Thus, a singular change in the aquatic environment from a widespread pollutant has the potential to generate a suite of consequences via changes in gill morphology. Critically, this suite of negative effects is likely most detrimental in salinized environments, where ionoregulatory demands are higher, which in turn should increase respiratory demands along with energy acquisition demands through foraging.Summary StatementChronic road salt exposure alters the functional morphology of gills in larval amphibians, potentially compromising osmoregulation, feeding, and respiration.

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Interactive effects of salinity and temperature acclimation on gill morphology and gene expression in threespine stickleback

Cited by 26 publications

References 63 publications

Conflict and Compromise: Using Reversible Remodeling to Manage Competing Physiological Demands at the Fish Gill

Conflict and Compromise: Using Reversible Remodeling to Manage Competing Physiological Demands at the Fish Gill

Gill remodelling during terrestrial acclimation in the amphibious fish Polypterus senegalus

Road salt compromises functional morphology of larval gills in populations of an amphibian

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