Elevated Salinity Rapidly Confers Cross-Tolerance to High Temperature in a Splash-Pool Copepod

Abstract

Accurate forecasting of organismal responses to climate change requires a deep mechanistic understanding of how physiology responds to present-day variation in the physical environment. However, the road to physiological enlightenment is fraught with complications: predictable environmental fluctuations of any single factor are often accompanied by substantial stochastic variation and rare extreme events, and several factors may interact to affect physiology. Lacking sufficient knowledge of temporal patterns of co-variation in multiple environmental stressors, biologists struggle to design and implement realistic and relevant laboratory experiments. In this study we directly address these issues, using measurements of the thermal tolerance of freshly collected animals and long-term field records of environmental conditions to explore how the splash-pool copepod Tigriopus californicus adjusts its physiology as its environment changes. Salinity and daily maximum temperature—two dominant environmental stressors experienced by T. californicus—are extraordinarily variable and unpredictable more than 2-3 days in advance. However, they substantially co-vary such that when temperature is high salinity is also likely to be high. Copepods appear to take advantage of this correlation: median lethal temperature of field-collected copepods increases by 7.5°C over a roughly 120 parts-per-thousand range of ambient salinity. Complementary laboratory experiments show that exposure to a single sublethal thermal event or to an abrupt shift in salinity also elicits rapid augmentation of heat tolerance via physiological plasticity, although the effect of salinity dwarfs that of temperature. These results suggest that T. californicus’s physiology keeps pace with the rapid, unpredictable fluctuations of its hypervariable physical environment by responding to the cues provided by recent sublethal stress and, more importantly, by leveraging the mechanistic cross-talk between responses to salinity and heat stress.

Hypoxia tolerance, but not low pH tolerance, is associated with a latitudinal cline across populations of Tigriopus californicus

“…californicus exhibit a phenotypic gradient for hypoxia survival, as has been documented for other environmental parameters in this species [ 14 , 20 ], and any phenotypic cline in low pH survival is substantially weaker. The latitudinal clines in thermal tolerance [ 14 , 20 – 23 ] and hypoxia tolerance inversely covary, which did not match our prior expectations. The oxygen-and capacity-limited thermal tolerance hypothesis predicts that an ectotherm’s thermal tolerance is limited by its ability to deliver oxygen to meet metabolic demand [ 25 , 27 , 85 – 87 ] although see also [ 88 – 90 ].…”

“…These geographic differences in habitat combined with low dispersal have resulted in populations with highly divergent genomes, particularly for mitochondrial DNA [ 17 – 19 ] ( S1 Table ). Common garden experiments have demonstrated local adaptation to thermal tolerance and some measures of salinity tolerance align with latitude, as southern populations are more tolerant of heat shock [ 20 – 23 ] and northern populations, which receive more rain, are generally more tolerant of extended periods at low salinity [ 14 , 15 , 24 ].…”

Developmental temperature, more than long‐term evolution, defines thermal tolerance in an estuarine copepod

“…Climate change may leave A. tonsa vulnerable to additional stressors, particularly in estuaries where periods of extreme salinity fluctuation coincide with warm temperatures (Heilmayer et al., 2008 ; Tolley et al., 2005 ). In corals and the tidepool copepod, Tigriopus californicus , increased salinity can impart additional thermal tolerance (Denny & Dowd, 2022 ; Gegner et al., 2017 ), while low environmental salinities are associated with narrowing thermal performance curves and elevated expression of heat shock proteins in the copepod Acartia tonsa (Peck et al., 2015 ; Petkeviciute et al., 2015 ), and reduced thermal tolerance in T. californicus (Kelly et al., 2016 ). Investigating the influence of temperature on salinity tolerance, and salinity on temperature tolerance in a widespread and numerically dominant copepod like A. tonsa will reveal the sensitivity of this impactful organism to future climate change.…”

Interactive effects of temperature and salinity on metabolism and activity of the copepodTigriopus californicus

“…Natural environments host a multitude of abiotic factors that can pose physiological challenges for organisms. These factors often covary, requiring organisms to respond to changes in multiple stressors at once (Denny and Dowd, 2022; Morris and Taylor, 1983). Marine environments are no exception, presenting various abiotic pressures from changes in temperature, oxygen concentration, pH, salinity, and more.…”

“…Although multiple stressors can interact in nearly all habitats, some such as the intertidal zone of rocky shores are characterized by especially unpredictable and extreme variation in multiple abiotic parameters, making them particularly useful model systems. In the intertidal zone these parameters include temperature, dissolved oxygen concentration, salinity, and pH (Denny and Dowd, 2022; Helmuth et al, 2002; Liguori, 2022; Morris and Taylor, 1983). Two of the most variable parameters in splashpools of the supratidal zone are salinity and temperature, which fluctuate over different timescales.…”