Short-term acclimation in adults does not predict offspring acclimation potential to hypoxia

Abstract

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 firstly investigated the effect of moderate, short-term environmental hypoxia (40% air saturation for one week) on metabolic performance in adults of an estuarine amphipod, and the fitness consequences of prolonged exposure. We then reared the offspring 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 effects in some species currently considered hypoxia tolerant.

Figure 1

Physiological performance of Gammarus chevreuxi under normoxia and moderate hypoxia. (a) Rates of mass-specific O₂ uptake, (b) heart rate, (c) ventilation rate, (d) expression levels (variance stabilised counts) of ten transcripts putatively identified as haemocyanin. ID represents the most significant 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 significant differences between groups (P < 0.05).

Figure 2

Chronic responses of juveniles and adult Gammarus chevreuxi to moderate hypoxia. (a) Mass-specific rates of O₂ uptake under acutely declining PO₂ and (b) critical PO₂ (or P_c) 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 offspring, and reared under the same conditions. Values are expressed as mean ± s.e.m. Letters above bars indicate significant differences between groups (P < 0.05).

Figure 3

Effect of moderate hypoxic exposure (40% air saturation) on measures of fitness in Gammarus chevreuxi. (a) Brood size, (b) developmental time, (c) egg volume and (d) size at hatching in F₁ individuals under normoxia (100% air saturation) and hypoxia (40% air saturation). Values are expressed as mean ± s.e.m. Letters above bars indicate significant differences between groups (P < 0.05).