Establishing the thermal threshold of the tropical mussel Perna viridis in the face of global warming

Highlights

• Upper and lower thermal limits of Perna viridis established.

• Hierarchy of thermal tolerance of P. viridis explored.

• Failure of higher level functions occurs earlier than lower ones.

• No significant hierarchical cold thermal tolerance observed.

• Narrow gap of optimal thermal window for mussel despite wide survival range.

Abstract

With increasing recognition that maximum oxygen demand is the unifying limit in tolerance, the first line of thermal sensitivity is, as a corollary, due to capacity limitations at a high level of organisational complexity before individual, molecular or membrane functions become disturbed. In this study the tropical mussel Perna viridis were subjected to temperature change of 0.4 °C per hour from ambient to 8–36 °C. By comparing thermal mortality against biochemical indices (hsp70, gluthathione), physiological indices (glycogen, FRAP, NRRT) and behavioural indices (clearance rate), a hierarchy of thermal tolerance was therein elucidated, ranging from systemic to cellular to molecular levels. Generally, while biochemical indices indicated a stress signal much earlier than the more integrated behavioural indices, failure of the latter (indicating a tolerance limit and transition to pejus state) occurred much earlier than the other indices tending towards thermal extremities at both ends of the thermal spectrum.

Introduction

Species ranges are defined by a series of physical and biological limits within which survival, growth and reproduction can occur. Towards the edges of their distribution range, species perform sub-optimally and their ability to compete for resources is reduced (Gaston, 2009). The physiological mechanisms limiting and adjusting cold and heat tolerance has gained further interest in the light of global warming and associated shifts in the geographical distribution of ectothermic animals (Pörtner, 2002). Understanding how these factors interact to define species ranges is crucial to our understanding of the response and fate of marine ecosystems in the face of climate change. Recent studies have documented climate-related mortality events (e.g. Wilkinson, 1999, Hughes et al., 2003), changes in population abundances (e.g. Sagarin et al., 1999, Ottersen, 2001), shifts in species range boundaries (Root et al., 2003), and phenological shifts in the timing of reproductive and migratory events (Kingsolver et al., 2002). However, most of these studies have not involved organisms living in the tropics.

Climate change has three different outcomes depending on the physiological response of the species or population in question (Fields et al., 1993). First, if environmental changes are sufficiently small, organisms may acclimatize to those conditions. Second, if environmental conditions exceed the ability of some, but not all, of the individuals to adapt to the environmental change, then natural selection may favour some genotypes already present in the population. In this case, the species range may be unchanged, but allele frequencies may vary (Hilbish, 1985, Kirby et al., 1997). Third, if conditions are sufficiently severe, all organisms in the population will die or emigrate and the entire species range will shift (Holt, 1990). While acclimatization may imply improved organismal performance, such phenotypic plasticity may not necessarily improve fitness. For example, plasticity often involves the re-allocation of resources to one trait at the expense of another (e.g. trade-off between growth and reproduction). Furthermore, phenotypic variation can strongly influence biological interactions within a community, often in complex and counterintuitive ways (Werner and Peacor, 2003).

It is hypothesized that, for a complex organism, a hierarchical series of tolerance prevails, ranging from systemic to cellular to molecular levels (Weibel et al., 1991), with highest sensitivity at the organismic level and wider tolerance windows at lower levels of complexity. Recent studies have increased understanding of the mechanisms underlying tolerance with the first line of sensitivities becomes apparent at the highest functional level possible, typically in the integrated function of ventilation and circulation for metazoan populations (Pörtner, 2001). If failure of individual molecular mechanisms is involved whole animal limits and the limits of these individual molecular mechanisms should be identical. In consequence, sensitivity levels of molecules, organelles, cells, tissues and the intact organism need to be distinguished to demarcate the optimum, pejus (pejus = getting worse) and pessimum (switch to anaerobic respiration) ranges with respect to thermal stress, as adopted from the law of tolerance (Shelford, 1931, Frederich and Pörtner, 2000) to elucidate the thermal tolerance of a species. From an ecological perspective, pejus rather than critical conditions are likely to reflect the upper and lower tolerance limits determining species distribution. It is therefore proposed that a suite of behavioural, physiological, and biochemical indices be adopted to assess the thermal tolerance of a particular species.

A total of 7 assays were employed here to elucidate the thermal tolerance of the green lipped mussel Perna viridis. Mussels are particularly suitable biomonitoring organisms as they are filter-feeders, and P. viridis is tolerant to a wide range of salinities and temperatures (Chatterji et al., 1984, Morton, 1987) and spawns continuously throughout the year (Tham et al., 1973), enabling them to be used as biomointoring agents (Philips, 1980; Tanabe, 2000). By comparing thermal mortality against biochemical indices (heat shock protein 70 and gluthathione levels), physiological indices (glycogen level, Ferric Reducing Antioxidant Power test, Neutral Red Retention) and behavioural indices (clearance rate or feeding efficacy), a hierarchy or sequence of thermal tolerance was therein elucidated, ranging from systemic to cellular to molecular levels.

The present work aimed to study the cellular, biochemical and molecular biomarkers in the foot muscle, mantle tissue and haemocytes of P. viridis and determine whether there is a hierarchy in their response to thermal stress. In the context of global warming the use of biochemical, cellular, molecular and physiological biomarkers could help in understanding the hierarchy in the cellular damage and dysfunction during thermal stress and in determining the threshold of temperatures inducing cell dysfunction. Also, such data may contribute in the understanding of how ‘environmental signals’ (e.g. air, surface and water temperatures) might translate into signals at the scale of the organism or cell (Pörtner and Farrell, 2008, Helmuth, 2009, Helmuth et al., 2010, Hofmann and Todgham, 2010).