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Short-Term Acclimation in Adults Does Not Predict Offspring Acclimation View metadata, citation and similar papers at core.ac.uk brought to you by CORE www.nature.com/scientificreportsprovided by Plymouth Electronic Archive and Research Library OPEN Short-term acclimation in adults does not predict ofspring acclimation potential to hypoxia Received: 17 August 2017 Manuela Truebano , Oliver Tills, Michael Collins, Charlotte Clarke, Emma Shipsides, Accepted: 5 February 2018 Charlotte Wheatley & John I. Spicer Published: xx xx xxxx The prevalence of hypoxic areas in coastal waters is predicted to increase and lead to reduced biodiversity. While the adult stages of many estuarine invertebrates can cope with short periods of hypoxia, it remains unclear whether that ability is present if animals are bred and reared under chronic hypoxia. We frstly investigated the efect of moderate, short-term environmental hypoxia (40% air saturation for one week) on metabolic performance in adults of an estuarine amphipod, and the ftness consequences of prolonged exposure. We then reared the ofspring of hypoxia-exposed parents under hypoxia, and assessed their oxyregulatory ability under declining oxygen tensions as juveniles and adults. Adults from the parental generation were able to acclimate their metabolism to hypoxia after one week, employing mechanisms typically associated with prolonged exposure. Their progeny, however, did not develop the adult pattern of respiratory regulation when reared under chronic hypoxia, but instead exhibited a poorer oxyregulatory ability than their parents. We conclude that species apparently hypoxia-tolerant when tested in short-term experiments, could be physiologically compromised as adults if they develop under hypoxia. Consequently, we propose that the increased prevalence of hypoxia in coastal regions will have marked efects in some species currently considered hypoxia tolerant. Hypoxia is one of the most rapidly changing environmental factors in coastal ecosystems, where oxygen tensions 1 (PO2) have decreased dramatically over the past decades as a result of increased anthropogenic nutrient input and climate change2. It is also now among the most widespread deleterious anthropogenic infuences, particularly in estuarine and marine environments3, which are ofen subject to seasonal or episodic hypoxia4. Physiologically, the ability to cope with hypoxia depends on the timescale of exposure. In coastal regions, hypoxia tends to be periodic, and there is evidence that physiological responses difer between cyclical and chronic exposure, as well as with severity and time-scales5,6. In the short term, hypoxia induces alterations in either metabolism (hypometabolism and/or recourse to anaerobic metabolism), or O2 uptake and transport (hyperventilation and/or increased perfusion), which ensure O2 delivery to tissues under conditions of low envi- 6,7 ronmental PO2 (reviewed in ). Afer prolonged exposure, these physiological mechanisms are replaced by more medium- to long-term modifcations, including increases in gill surface area, increased concentration and/or 6,7 afnity of O2-carrying molecules, or a combination of these . As the extent and duration of hypoxic events are predicted to intensify8, it is unclear whether aquatic organisms equipped with mechanisms to cope physiolog- ically with acute and short-term hypoxia will also be able to cope with prolonged or chronic exposure to even moderately low PO2. Te increase in extent and duration of hypoxic events in coastal regions means that aquatic invertebrates with rapid generation times will inevitably be exposed to at least moderate hypoxia across their life cycle, yet little 9 attention has been paid to the efect of rearing animals in low PO2 (although see ). Te ability to maintain O2 supply upon chronic exposure to low PO2 during the whole life cycle, will determine the ability of aquatic fauna to survive, grow and reproduce successfully. Understanding the physiological mechanisms underpinning this ability of aquatic organisms to cope with, acclimate and adapt to reduced PO2 is essential if we are to make predictions about the biological and ecological impacts of increasing hypoxia in coastal regions. We investigated the physiological mechanisms associated with the ability of an aquatic invertebrate to cope with moderate hypoxia in the short-term, and to test for efects of chronic exposure to moderate hypoxia across Marine Biology and Ecology Research Centre, Plymouth University, Plymouth, PL4 8AA, UK. Correspondence and requests for materials should be addressed to M.T. (email: [email protected]) SCIENTIFIC REPORTS | (2018) 8:3174 | DOI:10.1038/s41598-018-21490-y 1 www.nature.com/scientificreports/ Figure 1. Physiological performance of Gammarus chevreuxi under normoxia and moderate hypoxia. (a) Rates of mass-specifc O2 uptake, (b) heart rate, (c) ventilation rate, (d) expression levels (variance stabilised counts) of ten transcripts putatively identifed as haemocyanin. ID represents the most signifcant annotation, (e) haemocyanin (λ = 335 nm) to protein (λ = 280 nm) ratios and (f) contribution to the total gill area of gills from each pereon segment. Gill form outlines from a representative adult male are given above the bars. Numbers identify pereopod of origin. Amphipods were exposed to either normoxic (100% air saturation) or hypoxic (40% air saturation) conditions for one week. Mechanisms investigated are those typically associated with responses to short-term (hours to days), (b–c) and prolonged (weeks to months), (d–f) exposure to hypoxia in crustaceans. Values are expressed as mean ± s.e.m. Letters above bars indicate signifcant diferences between groups (P < 0.05). its life cycle. First, we investigated the efects of short-term (one week) exposure of adults to hypoxia on metabolic performance, as well as the mechanisms underpinning their response. Second, we compared the oxyregulatory ability of these adults, with that of juveniles and adults bred and reared under hypoxic conditions, whose parents were also kept under those conditions at the time of mating. Tird, we investigated the ftness consequences of exposure to moderate hypoxia. Gammarid amphipods are good models as they are abundant in coastal and estuarine areas where they are major components of the food web10. Te short-term hypoxic response has been documented for a number of gammarid species11–16 and varies with environmental history, with species inhabiting highly variable habi- tats exhibiting the greatest tolerance and best physiological performance13,17. Consequently, the brackishwater Gammarus chevreuxi18 was chosen for study, as it inhabits estuaries, where it experiences marked fuctuations in salinity, temperature and PO2. Results Mechanisms underpinning the ability to maintain metabolic performance in adults exposed to −1 short-term hypoxia. Exposure to moderate hypoxia (40% air saturation or approx. 2.6 mL O2 L ) for one week did not signifcantly afect the mass-specifc rate of oxygen uptake in G. chevreuxi (Fig. 1a). Te maintenance of oxygen uptake was accompanied by a signifcant decrease in heart rate (Fig. 1b, t-test, t12 = −2.96, P = 0.012) but no signifcant changes in ventilation (Fig. 1c). Exposure to moderate hypoxia for one week signifcantly SCIENTIFIC REPORTS | (2018) 8:3174 | DOI:10.1038/s41598-018-21490-y 2 www.nature.com/scientificreports/ Figure 2. Chronic responses of juveniles and adult Gammarus chevreuxi to moderate hypoxia. (a) Mass- specifc rates of O2 uptake under acutely declining PO2 and (b) critical PO2 (or Pc) of F0 adults (n = 6), F1 juveniles (n = 5) and F1 adults exposed to normoxic (100% air saturation) and hypoxic (40% air saturation) conditions. Individuals from the F1 generation were bred from parents exposed to the same treatment as their ofspring, and reared under the same conditions. Values are expressed as mean ± s.e.m. Letters above bars indicate signifcant diferences between groups (P < 0.05). afected the expression of ten genes putatively identifed as haemocyanin, with one gene signifcantly downregu- lated under hypoxia, while the remaining nine were signifcantly upregulated (Fig. 1d, Table S1). Tere were no signifcant diferences in haemocyanin to protein ratios (Fig. 1e), total gill area, total lamellar area contribution to total gill area, individual gill contribution to total gill area (Fig. 1f) between individuals exposed to normoxia and those exposed to moderate hypoxia for one week. Efects of chronic exposure to hypoxia across the life cycle. Exposure to hypoxia for one week did not afect rates of mass-specifc O2 uptake or critical PO2 (Pc or the point at which an individual loses res- piratory independence when exposed to acutely declining PO2) of F0 amphipods. Juvenile F1 amphipods bred from hypoxia-exposed parents and reared under hypoxic conditions showed greater rates of O2 uptake (Fig. 2a, ANOVA, F2,27 = 41.67, P < 0.001) and Pc (Fig. 2b, ANOVA, F2,27 = 23.58, P < 0.001) than their parents, irrespec- tive of the experimental treatment. When these F1 juveniles became sexually mature, i.e. adults, rates of O2 uptake and Pc were not signifcantly diferent from those of their parents in individuals reared under normoxia. However, in F1 adults reared under hypoxia from hypoxia-exposed parents, rates of O2 uptake were signifcantly lower than those of their parents (Fig. 2a, ANOVA, life cycle stage, F1,27 = 41.67, P < 0.001, O2 regime x life cycle stage F1,27 = 4.26, P = 0.026) and Pc signifcantly higher (Fig. 2b, ANOVA, life cycle stage, F1,27 = 23.58, P < 0.001, O2 regime x life cycle
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