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School of Biological Sciences, Washington State University, Pullman, Washington 99164
Dense biological communities on sulfide structures at deep-sea hydrothermal vents survive in one of Earth’s most extreme environments. The thermotolerance of vent animals dwelling on sulfide chimneys in the Northeast Pacific was determined by maintaining them in pressurized chambers under controlled temperature and chemical conditions. Observations indicated that lethal temperature correlates strongly with distributions observed in nature. One species studied, the alvinellid sulfide worm Paralvinella sulfincola, exhibited a thermal limit of 50–56 °C. Since observations of survival under controlled conditions are the only unambiguous means of demonstrating that an animal can tolerate a given environmental condition, the documented thermal limit for metazoan life at hydrothermal vents should be considered to be above 45 °C, but less than 60 °C.
Although the biology of hydrothermal vents has been actively investigated over the past 20 years, delineating linkages between the physical environment and the biota has been difficult. Gradients and temporal changes are pronounced. Therefore, to know what conditions a vent organism routinely encounters, measurements would ideally be conducted with spatial resolution at the sub-centimeter level, with temporal resolution over the course of days to weeks, and without modifying fluid flow by the presence of the sensor or submersible. Consequently, investigators are generally cautious in inferring physiological tolerance from environmental measurements. A recent study presents environmental data suggesting that Alvinella pompejana, a vent-chimney alvinellid worm, lives under sustained temperatures of 60 °C, which could make it the Earth’s most thermotolerant metazoan (1). However, steep thermal gradients and the difficulty of sampling fragile alvinellid tubes from a submersible have raised questions about the validity of these conclusions (2). For animals inhabiting less remote environments, corroborative evidence has often come from laboratory investigations of live animals. Such an approach has not been extensively used in studies of vent animals due to the requirement that experiments be conducted at high pressure. However, this kind of evidence is necessary to determine actual physiological limits. Documented survival under controlled conditions provides unambiguous evidence for thermotolerance. In the present study, this type of direct approach was taken to investigate the thermal tolerance of several species of vent animals.
Some of the sulfide-chimney assemblages at the Juan de Fuca and Explorer ridges in the Northeast Pacific are ideal for investigation of environmental tolerance since the dominant invertebrates, unlike those from other vent systems, are small and can fit in relatively inexpensive pressure vessels. Pressures at these sites (depths 1500–1800 m) are moderate, making it easier to maintain in situ pressure in experiments, and most organisms are motile, allowing behavioral investigations. In the present study, thermal limits were investigated for four abundant species of chimney invertebrates: the paralvinellids Paralvinella sulfincola and P. palmiformis, the limpet Lepetodrilus fucensis, and the snail Depressigyra globulus.
The distributions of these organisms on vent chimneys were described by Sarrazin et al. (3) and exhibit a "zonation" pattern of distinct invertebrate assemblages (named I through V) that differ in temperature and flow characteristics (3). Assemblage I, closest to hot vent fluids, consists almost entirely of P. sulfincola, which suggests that this species may be the most thermotolerant metazoan at Northeast Pacific vents. The second warmest assemblage, assemblage II, is dominated by P. sulfincola and P. palmiformis. The gastropods L. fucensis and D. globulus are also found in assemblage II, but are more common, and dominant, where the influence of venting is weaker (assemblages III–V). It is not clear what factors govern the distribution of organisms on sulfide structures. It has been postulated that tolerance to abiotic factors such as high temperature or hydrogen sulfide may be important regulators, but analysis of available environmental data and faunal distributions indicates that less than 30% of the variance in species distribution can be accounted for by abiotic factors that have been measured so far (4). If thermal tolerance is a factor governing distributions, then thermotolerance should be highest in P. sulfincola, followed by P. palmiformis, then L. fucensis and D. globulus. Specimens of P. sulfincola were collected from assemblage I, P. palmiformis from assemblage II and III, and gastropods from assemblage III. Differences in thermal tolerance among collections were not tested for. It is likely that further study could reveal acclimation to microhabitat conditions.
Observations of mixed assemblages of these species in pressurized chambers subjected to temperature increases are summarized in Figure 1. Each data point shown represents the outcome of a single experiment in one pressure chamber. The following endpoints were measured: (1) activity at experimental temperature by one or more individuals, with continued activity following return to low temperatures; (2) obvious reduction or cessation of activity, with restoration of activity following return to low temperatures; (3) activity at experimental temperature, but no activity at higher temperatures and no activity after return to low temperature in all individuals; or (4) no activity in all individuals, with no return of activity at lower temperatures. In some cases, category 2 was not readily observable; i.e., D. globulus appeared to exhibit high activity or none at all. In some trials, the threshold temperature at which activity ceases was not monitored. In these cases, animals exhibited no activity at a given temperature, but the threshold may have been lower. These instances were designated as category 4. Experiments consisted of a temperature increase (10 °C per hour) followed by return of temperature to 10–15 °C. In some cases, multiple experiments (at sequentially higher maximum temperatures) were conducted on the same sets of individuals (for D. globulus, L. fucensis, and P. palmiformis, 9 of 23, 8 of 17, and 2 of 8 experiments were from individuals exposed to two or three experimental temperature increases; all other experiments and all P. sulfincola experiments consisted of a single elevated temperature exposure). It is possible that exposure of animals to more than one temperature increase could have resulted in lower thermal limits for activity in those experiments.
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http://www.wsu.edu/~rlee/sulfideworm/psulf.html
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It is possible that experimentally determined temperature limits underestimate the tolerance shown in situ. This possibility is difficult to assess, but will be addressed in future tests of different conditions in pressure incubations (e.g., low pH, elevated pCO2) and experiments with animals recovered under pressure in pressurized recovery devices. In addition, trials of paralvinellid worms were conducted with their mucus tubes removed. It is possible that these tubes, which also contain mineral deposits, may provide some thermoprotective benefit. When animals are brought to the surface and repressurized, survival appears to be indefinite. At 1 atm, survival was a few days to weeks depending on species, indicating that pressure is required for long-term maintenance. Experiments in my laboratory and elsewhere have shown that vent animals collected from these and other sites survive for months in pressure chambers, even with periodic depressurization and repressurization to clean chambers or remove specimens. Additional study is underway to determine how long animals can tolerate sustained (several days) and transient (several minutes) exposure to experimental treatments as well as behaviorally preferred temperatures.
The limit of aquatic metazoan life is generally thought to be around 45 °C. The results presented here for P. sulfincola represent the first conclusive evidence that a vent animal tolerates temperatures that exceed 40 °C. The alvinellid Alvinella pompejana had previously been reported to be the Earth’s "hottest" living metazoan, based on a finding of sustained temperatures of 60 °C in occupied A. pompejana tubes (1). In addition, a single individual of A. pompejana had been observed to survive brief exposure to 105 °C when it crawled onto a submersible’s high-temperature probe (5). These findings are at odds with biochemical evidence indicating that the structure and function of enzymes and other macromolecules of A. pompejana are perturbed at temperatures of 50 °C or below (2, 6–10). The only previous study to directly investigate the thermal limits of live vent polychaetes shows that Hesiolyra bergi, which lives in the A. pompejana environment, does not tolerate temperatures above 40 °C (11). Thus the thermal limit of alvinellids remains a contentious issue. While extreme temperatures may be present in the alvinellid environment, alvinellids may inhabit cooler microenvironments or receive only transient pulses of extreme temperature, perhaps on the order of seconds. This disagreement may never be resolved. Unlike P. sulfincola, A. pompejana has not yet survived collection and recovery.
P. sulfincola may be as thermotolerant as A. pompejana since it exhibits properties of high enzyme thermostability (12) and inhabits a similar niche on sulfide structures. Temperatures at P. sulfincola tube openings range as high as 80–90 °C (S.K. Juniper, University of Quebec at Montreal, pers. comm.). Thus the data presented here are probably representative of tolerances exhibited by animals living at the limits for metazoan life at deep-sea vents. Pressurized experiments are the only unambiguous means of testing for survival under documented temperature. A combination of detailed environmental measurements, biochemical studies, and observation under controlled conditions is needed to reliably assess the thermal limits of vent fauna. The investigation of highly thermotolerant metazoans at deep-sea vents will remain an exciting area of investigation. The results shown here place the upper limit of aquatic animal life in the range of 45–55 °C.
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  S. W. Mills, L. S. Mullineaux, and P. A. Tyler Habitat Associations in Gastropod Species at East Pacific Rise Hydrothermal Vents (9{degrees}50'N) Biol. Bull., June 1, 2007; 212(3): 185 - 194. [Abstract] [Full Text] [PDF]
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