Thermal Physiological Traits and Plasticity of Metabolism Are Sensitive to Biogeographic Breaks in a Rock-Pool Marine Shrimp Aura M
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© 2018. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2018) 221, jeb181008. doi:10.1242/jeb.181008 RESEARCH ARTICLE Thermal physiological traits and plasticity of metabolism are sensitive to biogeographic breaks in a rock-pool marine shrimp Aura M. Barria1, Leonardo D. Bacigalupe2, Nelson A. Lagos3 and Marco A. Lardies1,* ABSTRACT gradually shapes the phenotypic responses of populations of a Populations of broadly distributed species commonly exhibit species along geographic clines (Castañeda et al., 2004; Lardies latitudinal variation in thermal tolerance and physiological plasticity. et al., 2011), leading to intraspecific variation in physiological traits This variation can be interrupted when biogeographic breaks occur in widely distributed species inhabiting contrasting environments across the range of a species, which are known to affect patterns of (Gaitán-Espitía et al., 2014; Stillman, 2002). In ectotherms, community structure, abundance and recruitment dynamics. Coastal performance traits (e.g. growth, reproduction, physiology) vary biogeographic breaks often impose abrupt changes in environmental with differences in TA, and this relationship can be described by a characteristics driven by oceanographic processes and can affect thermal performance curve (TPC; Angilletta, 2009; Huey and the physiological responses of populations inhabiting these areas. Berrigan, 2001) that includes three parameters: (1) critical thermal Here, we examined thermal limits, performances for heart rate minimum (CTmin), (2) critical thermal maximum (CTmax) and (3) and plasticity in metabolic rate of the intertidal shrimp Betaeus optimum temperature (Topt). Specifically, CTmin and CTmax emarginatus from seven populations along its latitudinal range represent the TA below and above which performance is at a (∼3000 km). The distribution of this species encompass two breaks minimum, and Topt represents the TA at which performance is along the southeastern Pacific coast of Chile: the northern break is maximized. As such, TPCs have been used to mechanistically characterized by sharp discontinuities in upwelling regimes, and the describe the variation in thermal tolerance among natural southern break constitutes a major discontinuity in water conditions populations of ectothermic species (Kingsolver et al., 2004; (temperature, pH, dissolved oxygen and nutrients), coastline Latimer et al., 2011; Schulte et al., 2011). The results of such topography and divergence of main oceanographic currents. For studies indicate that the parameters of TPCs usually co-vary along B. emarginatus, we found higher plasticity in metabolism at the sites geographic clines (e.g. latitude), reflecting the ability of ectotherms sampled at the biogeographic breaks, and at the site subjected to to adapt, at least in part, to their environments (Fangue et al., 2006; seasonal upwelling. The variation in metabolic rate was not consistent Klok and Chown, 2003; Lardies et al., 2004b). with increasing latitude and it was not affected by breaks. The The metabolic rate (MR) of an organism is linked to its pattern of ‘ lower and upper thermal limits were lower in populations around energy use, and as such, represents a holistic measure of the pace of ’ breaks, although the optimum temperature decreased towards life (Gillooly et al., 2001), and is suggested to reflect the energetic higher latitudes. Overall, whereas thermal limits and plasticity of cost of adaptation to a particular thermal environment (Clarke, metabolism are related to biogeographic breaks, metabolic rate is 2003; Clarke and Fraser, 2004). The relationship between MR and not related to increasing latitude or the presence of breaks in the TA also varies systematically across the ranges of ectotherms, in sampled range. concert with environmental gradients (Addo-Bediako et al., 2002). Two contrasting patterns of geographic variation have been KEY WORDS: Intraspecific variation, Thermal limits, Intertidal, described for the MRs of ectotherms (Bozinovic et al., 2011; Upwelling, Heart rate, Thermal performance curve, Reaction norm Burton et al., 2011). One body of evidence indicates that populations at lower latitudes, experiencing warmer temperatures INTRODUCTION throughout the year, exhibit higher MRs than their conspecifics at Because of its close relationship with physiological performance, higher/colder latitudes (Angilletta, 2001; Barria and Bacigalupe, ambient temperature (TA) plays a key role in determining the 2017; Lardies et al., 2004a; Peck, 2002). In contrast, the metabolic geographic distribution of ectotherms (Pörtner, 2001; Sunday et al., cold adaptation (MCA) hypothesis states that at equivalent TA, the 2012), as it is usually correlated with their upper and lower limits of MR of ectothermal species and populations from cold climates is thermal tolerance and physiological sensitivity (Sunday et al., greater than that of their warm-climate relatives (Addo-Bediako 2011). Also, it is thought that TA imposes selective pressure that et al., 2002; Gaston et al., 2009; Jacobsen and Brodersen, 2008). This compensation for low TA has been thought to be a general evolutionary adaptation of ectotherms from high latitudes or 1Departamento de Ciencias, Facultad de Artes Liberales, Universidad Adolfo altitudes (Chown and Gaston, 1999; Gaston et al., 2009). Ibañez, Diagonal Las Torres 2640, Peñalolen, Santiago 7941169, Chile. 2Instituto de Ciencias Ambientales y Evolutivas, Facultad de Ciencias, Universidad Austral However, although some studies support the MCA hypothesis for de Chile, Casilla 567, Valdivia 5110566, Chile. 3Centro de Investigacióne terrestrial insects (Addo-Bediako et al., 2002; Gaston et al., 2009), Innovación para el Cambio Climático, Facultad de Ciencias, Universidad Santo other authors have failed to find an increase in metabolism at lower Tomás, Ejército 146, Santiago 8370003, Chile. TA in marine organisms (Clarke, 1991; Rastrick and Whiteley, *Author for correspondence ([email protected]) 2011; Steffensen, 2002). The capacity of marine intertidal ectotherms to adjust their A.M.B., 0000-0001-5680-4890; L.D.B., 0000-0002-8141-2802; N.A.L., 0000- 0002-5886-1984; M.A.L., 0000-0003-3525-1830 physiological response to daily and seasonal fluctuations of environmental variables can define not only their vertical Received 16 March 2018; Accepted 31 July 2018 distributions, but also their geographical ranges (Pörtner, 2001; Journal of Experimental Biology 1 RESEARCH ARTICLE Journal of Experimental Biology (2018) 221, jeb181008. doi:10.1242/jeb.181008 et al., 2018 in press). In broadly distributed species, biogeographic List of symbols and abbreviations breaks might be contained in their range, and populations located in CTmax critical thermal maximum these areas could exhibit differences in abundance (Lancellotti and CTmin critical thermal minimum Vásquez, 1999; Sink et al., 2005), population dynamics (Broitman fH heart rate et al., 2001; Navarrete et al., 2008; Rivadeneira et al., 2002; Staaf MCA metabolic cold adaptation et al., 2010), and also in their phenotypic response (Lardies et al., MR metabolic rate SST sea surface temperature 2008; Ragionieri et al., 2009; Sanford et al., 2003). However, the TA environmental temperature environmental variability at biogeographic breaks has been poorly Topt optimum temperature related to the physiological capacities and plasticity of broadly TPC thermal performance curve distributed species. Two main biogeographic breaks have been reported along the range of the intertidal shrimp Betaeus emarginatus (H. Milne Sunday et al., 2011). Along latitudinal gradients, local adaptation to Edwards 1837) (Fig. 1) on the southeastern Pacific coast of Chile different environmental regimens can lead to differences in thermal (Camus, 2001). The northern break is located around 30–32°S tolerance and physiological plasticity among populations of broadly and is characterized by sharp discontinuities in upwelling regimes distributed species (e.g. Fangue et al., 2006; Gaitán-Espitía et al., (Thiel et al., 2007). The southern break, around 42°S, where the 2013, 2014; Gardiner et al., 2010; Lardies et al., 2011; Pörtner, geomorphology of the coastline changes from a continuous, almost 2001). In general, the scope of physiological plasticity is usually straight line to a fragmented one, is characterized by inner seas, bays proportional to the magnitude of variation in the TA that a species and channels, and is where the West Wind Drift over the Pacific experiences in their native habitat: populations inhabiting more Ocean splits into the northern Humboldt Current and the southern variable thermal environments (i.e. higher latitude) are expected to Cape Horn Current (Camus, 2001; Thiel et al., 2007; Montecino have broader tolerance limits and acclimation capacities than and Lange, 2009; Silva et al., 2009; Waters, 2008), the intensity of individuals inhabiting more stable environments (Calosi et al., which varies throughout the year, inducing a higher environmental 2010; Chown et al., 2004; Ghalambor et al., 2006; Janzen, 1967; heterogeneity in this area. As such, these breaks define three Naya et al., 2011; Stevens, 1989). Environmental variability biogeographic provinces: (1) the (northern) Peruvian province increases toward higher latitudes, and it is also high in coastal (from 4 to 30°S), (2) the (southern) Magellanic province (from ocean areas placed in biogeographic breaks, where geological, between 41 and 43°S to 54°S) and (3) an intermediate