Mechanistic studies on the physiology of CO2 tolerance in cephalopods.

Hu, Marian Yong-An (2011) Mechanistic studies on the physiology of CO2 tolerance in cephalopods. (Doctoral thesis/PhD), Christian-Albrechts-Universität, Kiel, Germany, 201 pp.

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Abstract

Beschreibung (original): Elevated environmental CO2 concentrations (hypercapnia) are a stressor that has lately received considerable attention: anthropogenic CO2 emissions are predicted to lead to a rise in surface ocean pCO2 from 0.04 kPa up to 0.08 - 0.14 kPa within this century. The increased hydration of CO2 changes seawater chemistry, causing a drop in ocean pH. This phenomenon has been termed “ocean acidification” (OA). Changes in aquatic CO2 partial pressure affect the physiology of all water breathing animals as the CO2 concentration in body fluids will increase as well in order to maintain a substantial outward directed diffusion gradient for CO2. Among the aquatic taxa some have been identified as rather sensitive species (e.g. less active calcifying species such as corals or echinoderms) whereas others (many active species such as adult fish and cephalopods) can tolerate high CO2 concentrations over long exposure times. It was shown that more tolerant organisms share the ability to compensate for a hypercapnia induced acidosis by actively accumulating bicarbonate and eliminating protons from their body fluids. This process requires the presence of an acid-base regulating machinery consisting of a variety of ion transporters and channels. Using in situ hybridization and immuno histochemical methods, the present work demonstrates that Na+/K+-ATPase (NKA), a V-type-H+-ATPase (V-HA), and Na+/HCO3- cotransporter (NBC) are co-localized in NKA-rich cells in the gills of cephalopods. Furthermore, mRNA expression patterns of these transporters and selected metabolic genes were examined in response to moderately elevated seawater pCO2 (0.16 and 0.35 kPa) over a time-course of six weeks in different ontogenetic stages. Our findings support the hypothesis that the energy budget of adult cephalopods is not significantly compromised during long-term exposure to moderate environmental hypercapnia. However, the down regulation of ion-regulatory and metabolic genes in late stage embryos, taken together with a significant reduction in somatic growth, indicates that in contrast to adult cephalopods early life stages are challenged more severely by elevated seawater pCO2. This increased sensitivity of cephalopod early life stages could be due to two primary reasons. The first is related to gill development: similar to the situation in fish and decapod crustaceans, the cephalopod gill is the most important site for ion-regulatory processes. During larval development, rudimentary gill structures occur at stage 20, and differentiate over the course of embryonic development as well as after hatching. This differentiation indicates that gas exchange and ion regulatory capacity might be fully activated only after leaving the protective egg capsule. This could partially explain the higher susceptibility of embryonic stages to environmental hypercapnia. The second reason for a higher sensitivity is due to the oviparous type of development in cephalopods. Cephalopod embryos are exposed to very low egg fluid pO2 values (<6 kPa, ca. 28% air saturation) and high pCO2 values (>0.3 kPa) under control conditions during the final phase of embryonic development. This is due to increasing metabolic rates and the egg casing acting as a diffusion barrier for dissolved gases. The present work demonstrates that environmental pCO2 is additive to the natural accumulation of CO2 in the perivitelline fluid (PVF). This almost linear increase of PVF pCO2 is necessary in order to conserve the CO2 diffusion gradient across the egg capsule that drives excretion of metabolic CO2 to the seawater. Thus, alterations in environmental pCO2 create a greater challenge to the developing embryo in comparison to juveniles or adults. Despite the lack of adult-like high capacity ion regulatory epithelia (e.g. gills or kidneys) the present work demonstrates for the first time that cephalopod embryonic stages exhibit convergent acid-base regulatory features compared to teleosts. Epidermal ionocytes scattered on skin and yolk sac appear to be responsible for ionic and acid-base regulation before gill epithelia become functionable. Acid-base regulatory capacities are important for fish and cephalopod embryos, due to the beforehand mentioned, challenging abiotic conditions inside the protecting egg capsule. These epidermal ionocytes were characterized via immunohistochemistry, in situ hybridization and vital dye staining techniques. Similar to findings obtained in teleosts NHE3-rich cells take up sodium in exchange for protons, illustrating the energetic advantage of NHE based proton excretion in marine organisms. Using in vivo electrophysiological techniques, it was proven that acid equivalents are secreted by the yolk and skin integument. The findings of the present work add significant knowledge to our mechanistic understanding of hypercapnia tolerance in marine organisms, as it demonstrates that cephalopods which were identified as powerful acid-base regulators in the context of ocean acidification already need to exhibit strong acid-base regulatory abilities during all phases of their life cycle. The convergence of key acid-base regulatory proteins in cephalopods and fish suggest that in a variety of marine ectothermic animals extracellular pH regulation mechanisms may follow common evolutionary principles.

Document Type: Thesis (Doctoral thesis/PhD)
Thesis Advisors: Melzner, Frank and Bleich, Markus
Keywords: Benthic Ecology; Biogeochemistry; Ocean acidification, Acid-base regulation, Cuttlefish, Squid; Ozeanversauerung, Säure-Baseregulation, Tintenfisch, Kalmar; Annette-Barthelt-Preis
Research affiliation: Kiel University > Faculty of Medicine > Institute of Physiology
OceanRep > GEOMAR > FB3 Marine Ecology > FB3-EOE-B Experimental Ecology - Benthic Ecology
Open Access Journal?: Yes
Projects: Annette-Barthelt-Preis
Date Deposited: 13 Jan 2012 10:53
Last Modified: 11 Jun 2015 08:04
URI: http://oceanrep.geomar.de/id/eprint/13481

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