Research Article: Chronic environmental stress enhances tolerance to seasonal gradual warming in marine mussels

Date Published: March 23, 2017

Publisher: Public Library of Science

Author(s): Ionan Marigómez, Maria Múgica, Urtzi Izagirre, Inna M. Sokolova, Peter P. Fong.


In global climate change scenarios, seawater warming acts in concert with multiple stress sources, which may enhance the susceptibility of marine biota to thermal stress. Here, the responsiveness to seasonal gradual warming was investigated in temperate mussels from a chronically stressed population in comparison with a healthy one. Stressed and healthy mussels were subjected to gradual temperature elevation for 8 days (1°C per day; fall: 16–24°C, winter: 12–20°C, summer: 20–28°C) and kept at elevated temperature for 3 weeks. Healthy mussels experienced thermal stress and entered the time-limited survival period in the fall, became acclimated in winter and exhibited sublethal damage in summer. In stressed mussels, thermal stress and subsequent health deterioration were elicited in the fall but no transition into the critical period of time-limited survival was observed. Stressed mussels did not become acclimated to 20°C in winter, when they experienced low-to-moderate thermal stress, and did not experience sublethal damage at 28°C in summer, showing instead signs of metabolic rate depression. Overall, although the thermal threshold was lowered in chronically stressed mussels, they exhibited enhanced tolerance to seasonal gradual warming, especially in summer. These results challenge current assumptions on the susceptibility of marine biota to the interactive effects of seawater warming and pollution.

Partial Text

With the advent of global climate change, rise in seawater surface temperature can severely affect coastal ecosystems [1,2]. Temperature elevation affects metabolic regulation in marine organisms and may induce thermal stress [3,4], which leads to reduced aerobic scope, depressed metabolism as well as disturbed physiological functions, reproduction and general health condition. As a result, less energy is allocated to growth, storage, defence and reproduction [4–6]. Furthermore, seawater warming acts in concert with contaminants and other stress sources operating in marine ecosystems [7,8].

Unless otherwise indicated, all chemicals and enzymes were purchased from Sigma- Aldrich (St. Louis, MO, USA), Roche (Indianapolis, IN, USA) or Fisher Scientific (Pittsburg, PA, USA) and were of analytical grade or higher.

Whereas elevated temperatures induced alterations beyond those caused by seasonal changes [27,50–52,56,58] in healthy mussels, adaptation to a polluted environment attenuated the effects of thermal stress in stressed mussels (Table 2). In comparison with healthy ones, stressed mussel populations (a) show adaptive modifications to survive in a stressed environment that may account for muted responses to thermal stress, (b) possess a high energy storage that partially contributes to alleviate thermal stress, and (c) are able to survive longer under the extremely elevated temperatures of 28°C than healthy mussel populations. As a whole, stressed mussels present lower thermal stress threshold but are considerably more tolerant to elevated temperature in the long-term than healthy mussels. Marine bivalves inhabiting polluted sites are believed to be more susceptible to thermal stress [11], which explains the lower thermal stress threshold presently found in stressed mussels in comparison with healthy mussels. However, environmental traits associated with polluted environments such as adaptation to chronic stress and eutrophication (resulting in high food availability) may alleviate these effects by providing additional energy supply to counteract the energetic requirements to deal with warming and enabling survival during prolonged thermal stress. Similar enhancement of temperature tolerance due to elevated food availability was shown in other populations from eutrophicated polluted estuaries, although this response depended on the food quality [77,78]. Moreover, gradual warming induces gonad resorption in healthy mussels, hampers the commencement of a new gametogenic cycle in fall and induces massive spawning in summer both in healthy and stressed mussels but much less markedly and at longer times in the latter. Therefore, the present study provides experimental evidence that tolerance to seasonal gradual warming may be enhanced in mussel populations chronically subject to environmental stress. This indicating that the current assumption that the interaction of multiple stressors would enhance the susceptibility of marine biota to seawater warming may not be universally true and can be modified by specific local conditions (especially energy and food availability).




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