Gills develop early in coral reef fishes: respiratory and ionoregulatory processes

Prescott, Leteisha A. (2019) Gills develop early in coral reef fishes: respiratory and ionoregulatory processes. Masters (Research) thesis, James Cook University.

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Abstract

Coral reef ecosystems are among those that are most heavily impacted by anthropogenic disturbances, including climate change, overfishing, and other activities resulting in habitat loss. Consequently, studies have found that fish exposed to these disturbances respond negatively, both behaviourally and physiologically. However, these studies have primarily focused on adult fishes; whereas early life stages – the seeds of adult populations – are substantially understudied. Nonetheless, early life stages are thought to be most vulnerable to environmental stress, owing to rudimentary organs and underdeveloped physiological systems. Processes that are likely to be impacted are those related to the respiratory (oxygen and carbon dioxide exchange) and ion/osmoregulatory (ion and water balance) systems because of potential mismatch between the environmental pressures and the pace at which these systems develop.

In fish, respiration and ion/osmoregulation are known to primarily occur at the gills; however, during early life stages, before the gills form, these physiological processes are maintained through cutaneous pathways. The transition of these processes from cutaneous (i.e., skin) to branchial (i.e., gill) has been thoroughly investigated in model species, such as the rainbow trout (Oncorhynchus mykiss), where it is thought that gills begin functioning for ion regulation (15 days post hatch; dph) before oxygen uptake (23-28dph). This information is not known for coral reef fishes. Although, this transition is thought to occur earlier in coral reef fishes than in temperate species, like the rainbow trout, because of the influence of warm temperatures and low oxygen levels on metabolic processes. In addition, this transition is thought to be energetically costly under ideal environmental conditions, and perhaps, further exacerbated by anthropogenic stressors. Developmental deficiencies to those systems could lead to reductions in whole organism performance and ecosystem health.

The following thesis investigates gill development in coral reef fish species with the aim to determine the onset of respiratory and ionoregulatory systems. This is the knowledge base needed to better predict how anthropogenic stress could affect coral reef ecosystems. To do this, two coral reef fish species (Acanthochromis polyacanthus and Amphiprion melanopus) were chosen. As pomacentrids, these two species belong to one of the most speciose coral reef fish families and are of high ecological importance. In addition, both are easily maintained in captivity, life cycles have been closed, genomes fully sequenced, and as a result, both are quickly becoming model laboratory species. This further highlights the importance of understanding the development of these basic but critical processes associated with respiration and ion regulation. The first experiments (Chapter 2) were designed to describe, in detail, the ontogeny of gill development in two coral reef fishes. I found gill tissues to form, in these two species, faster than in any other studied fish to date. Specifically, all gill structures were apparent prior to hatching. The onset of gill development may be a critical developmental window, as it is often associated with high mortality, and therefore, should be a milestone that future studies consider when investigating coral reef fish populations.

The accelerated developmental pace observed in these two coral reef fish species is perhaps related to the environmental conditions they experience (e.g., warm water temperatures during the day and low oxygen levels at night) that demand respiratory efficiency. Theoretically, the onset of gill development should coincide with increased oxygen requirements beyond what can be provided through cutaneous pathways (i.e., the oxygen hypothesis). In chapter 3, I tested this hypothesis by measuring the oxygen uptake of Amphiprion melanopus and Acanthochromis polyacanthus over their embryonic development. When fish start using their blood (i.e., using haemoglobin; Hb, the oxygen carrying protein found in nearly all vertebrate species) to bind oxygen from the environment and deliver it to their tissues, they are presumably using the gills to do this. If I inhibit the function of Hb (e.g., using phenylhydrazine (PHZ) to breakdown Hb), the fish is then only able to rely on cutaneous pathways to uptake oxygen. Therefore, when Hb is required to enhance oxygen transport, this should coincide with the onset of gill function for respiration. I found that, prior to hatching, embryos are able to satisfy oxygen demand via cutaneous pathways (i.e., in the absence of hemoglobin) alone. Upon hatching, cutaneous respiration was insufficient, suggesting that gills are critical for respiration after this stage. Linking these physiological findings with observations of gill development in coral reef fish obtained in chapter 2, my results suggest that the rapid onset of gill formation during embryogenesis is essential to meet oxygen requirements of fish larvae immediately after hatching. However, the presence of gill tissue before it is required for branchial oxygen uptake suggests that other processes may be initiating and requiring gill formation pre-hatch.

The ionoregulatory hypothesis suggest that cutaneous processes for ion/osmoregulatory balance become insufficient before those for respiration because transporters are localised within specialised cells. Therefore, surface area to volume ratios (SA/V) will limit ion exchange before limiting respiration. In chapter 4, I used immunohistochemistry to observe the primary enzymatic ion exchanger, Na+ K+ ATPase (NKA), on the skin, yolk-sac, and the gills in developing embryos of two coral reef fish species to determine when ion regulation processes begin. I found NKA to first appear on the skin and yolk-sac at 1-2 days post fertilization (dpf) and on the gill filaments at 3-5 dpf. My study is the first to provide evidence that coral reef fishes use NKA external to the gills, i.e., through cutaneous pathways. Additionally, these fishes show an accelerated developmental pace of ion regulation, with the earliest appearance of NKA on the skin and the gills in any species investigated to date. The early appearance of ionoregulatory cells on the gills before the formation of lamellae and before the onset of branchial oxygen uptake suggests that ion regulation is the primary driver underpinning gill development in these fishes. My findings support the ionoregulatory hypothesis.

The first critical developmental window for coral reef fishes is prior to hatching, when gills begin to form. Therefore, anthropogenic stressors or other environmental perturbations that could disrupt gill development pre-hatch may preclude healthy adult populations and coral reef ecosystems. Here, I emphasize that embryonic life stages must be considered when investigating the impacts of anthropogenic stressors on coral reef fishes. Processes performed by the gills, if impeded, could have negative cascading effects throughout development and into adulthood. Overall, understanding the structure and function of gills and how and when they develop is essential to understanding fish ecology and evolution, but can also be key to effectively managing fish populations in a changing world.

Item ID: 60894
Item Type: Thesis (Masters (Research))
Keywords: coral reef fishes, gills, ion regulation, oxygen consumption
Copyright Information: Copyright © 2019 Leteisha A. Prescott.
Date Deposited: 06 Nov 2019 04:24
FoR Codes: 06 BIOLOGICAL SCIENCES > 0602 Ecology > 060203 Ecological Physiology @ 60%
06 BIOLOGICAL SCIENCES > 0602 Ecology > 060205 Marine and Estuarine Ecology (incl Marine Ichthyology) @ 40%
SEO Codes: 97 EXPANDING KNOWLEDGE > 970106 Expanding Knowledge in the Biological Sciences @ 100%
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