Effect of acclimation temperature on thermal tolerance between American lobster (Homarus americanus) collected in different lobster fishing areas in Atlantic Canada
Abstract
The American lobster fishery is the most economically significant commercial fishery in Atlantic Canada and takes place in waters that are warming due to climate change. Lobster are poikilotherms that tolerate a wide range of seasonal temperatures with an optimal range of 12–18 °C. Lobster in the Canadian Maritimes may be naturally acclimated to a wide range of temperatures and thus, could have a wide range of thermal tolerance that may be distinct across regions. The present study used non-invasive open-source tools to explore differences in thermal tolerance in real time between geographically separated lobster populations from around the Canadian Maritimes. Lobsters were acquired from six lobster fishing areas in the Canadian Maritimes and acclimated to either warm (15 °C) or cold (5 °C) water for two weeks before the onset of thermal trials. Geographic origin was not a significant predictor of estimated thermal maximum, while acclimation temperature was a significant predictor. These results suggest that thermal tolerance is more strongly linked to acclimation temperature than to geographic region.
Introduction
Ocean temperatures in the Northwest Atlantic have increased at a rate of 0.03 °C year−1 over the past four decades and are warming faster than the global average of 0.01 °C year−1 (Wu et al. 2012; Forsyth et al. 2015; Pershing et al. 2015). Ocean temperatures in Canada are projected to continue increasing over the 21st century, and the waters around Nova Scotia are predicted to warm faster than the rest of the country under all emissions scenarios (Greenan et al. 2018; Lavoie et al. 2020). Warm water bottom temperature anomalies have also increased in offshore waters around Nova Scotia since the 1980s due, in part, to the influence of the Gulf Stream relative to the Labrador current (Fisheries and Oceans Canada 2019).
The American lobster (Homarus americanus H. Milne-Edwards, 1837) fishery is the most profitable commercial fishery in Atlantic Canada, valued at approximately $2 billion in 2021 (Fisheries and Oceans Canada 2022) and takes place in warming nearshore and offshore areas. There are 41 discrete lobster fishing areas (LFAs) (Lobster Council of Canada 2020) that are further sub-divided into a total of 47 unique zones (Government of Canada 1985; Serdynska and Coffen-Smout 2017). Within LFAs, lobster inhabit waters with a wide range of seasonal temperatures, from −1 to 26 °C (Lawton and Lavalli 1995; Quinn 2017); however, laboratory studies indicate a preferred temperature range between 12 and 18 °C for adults (Crossin et al. 1998). Within this temperature range, lobster larvae display greater survival and faster growth (MacKenzie 1988; Annis et al. 2013; Quinn 2017), whereas temperatures above 20 °C have been linked to higher physiological stress, disease, and mortality in both adults and larvae (Pearce and Balcom 2005; Glenn and Pugh 2006). Increases in temperature also correspond to an increase in metabolism for all poikilotherms, including lobster (Jury and Watson 2000).
Early work tested the thermal limits of American lobster collected in the nearshore waters of eastern New Brunswick in the Gulf of St. Lawrence, Prince Edward Island, southwestern Nova Scotia, and Cape Breton Island (McLeese 1956). McLeese (1956) found that the upper thermal limit for American lobster could be increased by approximately 2.7 °C following a 3-week acclimation period at 5 °C versus 15 °C. This work was foundational in establishing a relationship between acclimation temperature and thermal tolerance in American lobster, but used a simple method to determine when lobsters were “dead”. McLeese (1956) considered American lobster to be “dead” when they could detect no movement from any part on close examination. In more recent years with newer technology, Camacho et al. (2006) demonstrated that temperature acclimation altered cardiac performance and critical thermal maximum in American lobster using an impedance converter connected to wires drilled through the carapace connected to the heart. Their findings supported earlier work of McLeese (1956), and Camacho et al. (2006) suggested that cold-acclimated lobster have a significant physiological advantage since they have a larger capacity for extending their upper thermal limit than warm-acclimated lobster and are living in conditions far below this limit.
In lobster, a beating heart is required to circulate haemolymph and deliver oxygen to the body. In vivo experimentation has demonstrated that lobster heartbeats can be detected using an impedance converter connected to wires inserted into the lobster carapaces (Worden et al. 2006). For this invasive in vivo experiment, lobster had to be isolated and maintained for at least 48 h with the impedance converter prior to experimentation, to reduce the stress of the insertion of the wires through the carapace and into the heart (Worden et al. 2006). Conversely, photoplethysmography (PPG) is a non-invasive technique that uses infrared (IR) light to measure changes in blood volume in real time (Challoner and Ramsay 1974). This technique was originally developed to monitor the heart rates of children under anaesthesia and has also been tested in the Green crab (Carcinus maenas) (Depledge 1984). A variety of PPG devices have been used to infer heartbeats in other decapod crustaceans such as spiny lobsters (Jasus edwardsii, Sagmariasus verreauxi, and Panulirus ornatus) (Oellermann et al. 2020), giant freshwater shrimp (Macrobrachium rosenbergii) (Ern et al. 2014), crayfish (Astacus astacus) (Fedotov et al. 2000), brown crabs (Cancer pagurus) (Maus et al. 2021), and Jonah crabs (Cancer borealis) (Kushinsky et al. 2019) in laboratory settings and in American lobster (H. americanus) in the wild (Gutzler and Watson 2022). The capacity to detect lobster heartbeats in vivo with non-invasive technology presents an exciting opportunity to investigate the effects of thermal acclimation on critical thermal maxima in real time.
While the work of McLeese (1956) and Camacho et al. (2006) were critical in establishing the relationship between thermal acclimation and thermal limits, they did not adequately address the potential effects of geographically separated lobster populations on thermal maxima. These populations may be adapted to local or regional temperatures (Benestan et al. 2016) and consequently, have different thermal maxima. The present study used PPG to identify periods of thermal stress in real time as indicated by irregular cardiac activity to explore differences in euthanasia temperature between geographically separated American lobster populations from LFAs around Nova Scotia, Canada acclimated to either warm (15 °C) or cold (5 °C) water.
Materials and methods
Animal husbandry
This work was performed under ACUC permit #2023-017. Commercial lobster harvesters acquired 240 (120 male and 120 female) American lobster in LFAs 24, 27, 31a, 33, 34, and 35 (Table 1, Fig. 1), that were sold to the researchers and brought to the Haley Institute at Dalhousie University, Truro, Nova Scotia and distributed into two seawater recirculating aquaculture systems (RAS) comprised of six, 1500 L circular tanks each. Male and female lobsters from each LFA were distributed evenly between the two RAS. Seawater was sourced from Halifax Harbour, pumped ashore to the Dalhousie University Aquatron Facility (Halifax, NS) and filtered through sand to exclude particles > 30 µm. Ambient seawater was cooled to 4 °C prior to use in the RAS. Water recirculated through one of two loops. Surface water was drawn from the tanks and returned to a sump tank in each loop. The first loop passed seawater through a 50 µm sand-filter followed by a trickle-down biological filter containing 1 m3 media. A head volume of water at the base of the biological filter stood 1.8 m above the floor and provided hydraulic pressure to oxygenate in-line with the out-flowing water before supplying water back to the rearing tanks. Nominal flow rate to each tank was 15 L min−1 and excess water was returned to the sump tank. The second loop passed water through a 6 kW heat pump and a foam fractionator before returning to a sump tank. Each holding tank was equipped with a double drain that allowed concentrated effluent to be purged to waste once daily. Water loss on each system was minimal, attributed to effluent purging and minor system water loss. Temperature and water flow to the biological filter were monitored continuously. Each RAS was provided <100 L d−1 of new water. Water chemistry was measured twice weekly using a LaMotte Spin Touch (LaMotte, Chestertown, MD, USA).
Fig. 1.
Table 1.
| LFA | Mean LFA annual bottom temperature (°C) ± SD | Sex | Number used | Mean weight (g) ± SE | Intake date |
|---|---|---|---|---|---|
| 24 | 2.39 ± 1.25 | F | 19 | 748.3 ± 9.3 | 06/30/2022 |
| 24 | 2.39 ± 1.25 | M | 19 | 713.1 ± 9.2 | 06/30/2022 |
| 27 | 4.01 ± 1.27 | F | 20 | 625.5 ± 12.0 | 07/05/2022 |
| 27 | 4.01 ± 1.27 | M | 19 | 627.9 ± 14.4 | 07/05/2022 |
| 31a | 3.11 ± 0.74 | F | 19 | 689.8 ± 11.7 | 05/17/2022 |
| 31a | 3.11 ± 0.74 | M | 19 | 712.5 ± 13.1 | 05/17/2022 |
| 33 | 5.45 ± 1.44 | F | 20 | 672.9 ± 2.6 | 05/17/2022 |
| 33 | 5.45 ± 1.44 | M | 19 | 657.8 ± 11.0 | 05/17/2022 |
| 34 | 6.05 ± 1.44 | F | 20 | 725.6 ± 6.1 | 05/17/2022 |
| 34 | 6.05 ± 1.44 | M | 19 | 718.3 ± 5.5 | 05/17/2022 |
| 35 | 7.34 ± 1.62 | F | 20 | 704.7 ± 12.8 | 07/05/2022 |
| 35 | 7.34 ± 1.62 | M | 14 | 686.8 ± 9.8 | 07/05/2022 |
Following a one-week acclimation period at 4 °C water temperature was raised by 2 °C d−1 until one RAS was maintained at 5 °C, while the other was maintained at 15 °C. Lobsters were acclimated to these temperatures for two weeks before the onset of experimentation. Dalhousie University staff performed twice daily health checks. Lobsters were not fed during acclimation (McLeese 1956) to mimic conditions in commercial lobster holding facilities.
All experimental groups (LFA*acclimation temperature) had 19 or 20 animals, except for warm-acclimated lobsters from LFA 35, which had 15. The lobster from LFA 35 were brought to the Haley Institute later than the others and may have been exposed to elevated water temperature prior to capture due to the timing of the LFA 35 fishing season. Lobsters tend to molt more frequently in warmer waters (Waddy et al. 1995; Mills et al. 2013; Schmalenbach and Buchholz 2013; Staples et al. 2019) and recently molted lobsters have softer shells, higher water content, and reduced meat yield which leads to reduced survivability during capture and transport (Thakur et al. 2017). In keeping with previous work (Camacho et al. 2006; Worden et al. 2006), only hard-shelled lobsters were used in the present study, which accounts for the lower numbers from the warm-acclimated group from LFA 35.
Heartbeat monitors
Custom lobster heartbeat monitors were built using a reactive infrared sensor (Adafruit, New York, NY, USA) connected to an EasyPulse v1.1 (Embedded-lab.com), controlled with an Arduino Uno R2 (Arduino, Turin, Italy). The reactive IR sensors were inserted through a 12 cm2 piece of silicone to facilitate mounting the sensor on the lobster via polyacrylamide glue (Gorilla Glue Company, Cincinnati, OH, USA) (Fig. 2). All code used for the heartbeat monitors is open-source and available (https://github.com/Ryan-Horricks/Heartbeat-multiple).
Fig. 2.
Thermal trials
A total of 12 thermal trials were conducted to determine the euthanasia temperature of American lobster. Two recirculating 147 L systems were used for the thermal trials. Each custom-built system comprised of a 64 L sump (Sterilite, Townsend, MA, USA) equipped with two Danner Supreme Mag-Drive 3 water pumps (Danner Manufacturing Inc., Islandia, NY, USA) that circulated aerated seawater into a 20.8 L baffle that cascaded into two stacked 31.2 L experimental tanks (Global Industrial, Port Washington, NY, USA) (Fig. 3). Each experimental tank was subdivided into 5 cells using plastic dividers (Global Industrial).
Fig. 3.
Lobster of both sexes originating from one LFA and acclimation temperature group (Table 1) were weighed, connected to a heartbeat monitor, and randomly distributed into the two experimental systems at the onset of each thermal trial. Seawater was heated from the acclimation temperature of each group in the sump at an average rate of approximately 0.15 °C min−1 ± 0.003 (mean ± SE) to a maximum temperature of 33 °C using a 1500 W titanium immersion heater (Aquameric, Montreal, QC) during the thermal trials. Temperature and dissolved oxygen in each experimental tank were monitored constantly and recorded every 5 min using digital thermometers (Veanic, Shenzen, CN) and U26-001 HOBO Data Loggers (Onset, Bourne, MA, USA), respectively. In compliance with a request from the animal care committee, all lobsters used in the present study were euthanized by severing the central nerve ganglion before they reached their true thermal maximum and euthanasia temperature was recorded. Lobsters were removed from the experimental tanks and euthanized when the heartbeat became irregular (e.g., Fig. 4) and animals voided their stomach contents. For several minutes following euthanasia all lobsters continued to move their legs and antennae and previous work (F. Clark, pers. comm. 2022) has shown that lobster hearts continue to beat in a similar manner following euthanasia by severing the central nerve ganglion.
Fig. 4.
Statistical analysis
All statistical analyses were conducted using R Version 4.3.3 (R Core Team 2024) and the “tidyverse” (Wickham et al. 2019) and “lubridate” (Grolemund and Wickham 2011) packages with a significance level of α = 0.05.
The non-parametric Kruskal–Wallis one-way Analysis of variance (ANOVA) was used to test for differences in weight and sex between different experimental groups and for the effect of weight, sex, LFA, and acclimation temperature on euthanasia temperature. Non-parametric tests were used as the data had unequal variance between groups and thus, violated the assumptions of ANOVA. A Kruskal–Wallis one-way ANOVA was used to test for differences in euthanasia temperature between the two acclimation groups.
Results
There were no significant differences in mean lobster weight between sexes (P = 0.464); however, there were significant differences by LFA (P = 2.11e-18) for the experimental animals. Despite the significant difference in mean lobster weight between LFAs, sex (P = 0.842), and weight (P = 0.456) were not significant predictors of euthanasia temperature. LFA was not a significant predictor of euthanasia temperature (P = 0.080) while acclimation temperature was (P = 1.802e-37) (Fig. 5). Warm-acclimated (15 °C) lobster had a mean euthanasia temperature of 29.6 °C ± 0.11 (mean ± SE) while cold-acclimated (5 °C) lobster had a mean euthanasia temperature of 25.7 °C ± 0.14 (mean ± SE).
Fig. 5.
Discussion
The present study explored the relationship between acclimation temperature and LFA origin on euthanasia temperature for American lobsters harvested in the Canadian Maritimes. In agreement with previous studies (McLeese 1956; Camacho et al. 2006), the present paper demonstrated that lobster acclimated to warmer temperatures (15 °C) have a significantly higher thermal maximum (29.6 °C ± 0.11 (mean ± SE)) than lobsters acclimated to colder temperatures (5 °C; 25.7 °C ± 0.14 (mean ± SE)), regardless of the LFA of origin. All six LFAs used in the present study have significantly different mean annual bottom temperatures that do not directly correspond to increasing latitude (Wang et al. 2018).McLeese (1956) identified differences in life history strategies for lobster in the Gulf of St. Lawrence and southwestern New Brunswick that they attributed to differences in oceanographic conditions between those regions, yet, found no differences in thermal maxima between lobster from those regions. The present study corroborates these findings. While there were significant differences in weight of lobster between LFAs used in the present study, this did not have a significant effect on euthanasia temperature. Indeed, the only significant factor determining euthanasia temperature was acclimation temperature. McLeese (1956) used acclimation temperatures of 5 and 15 °C on American lobster originating from different geographic regions to identify temperatures of 24–25.7 and 27.8–28.4 °C, respectively, that killed 50% of animals within 48 h. Camacho et al. (2006) used acclimation temperatures of 4 and 20 °C on American lobster to identify changes in cardiac function at 25.4 and 30–30.3 °C, respectively. While McLeese (1956) and Camacho et al. (2006) used different endpoints and methods to assess thermal tolerance limits than the present study, they identified thermal tolerance limits that were remarkably close to the euthanasia temperatures presented here.
This research provides additional insight into the potential for thermal adaptation under climate change and impacts for considering lobster sensitively under climate change vulnerability assessments. Climate change and warming ocean waters pose many threats to poikilotherms, animals that are unable to metabolically self-regulate body temperature, like the American lobster. Lobsters in warmer waters tend to reach maturity at smaller sizes and younger ages, which may potentially reduce the overall fecundity and recruitment of the population (Waller et al. 2017). An analysis of 30 years of survey data collected from southern New England and the Bay of Fundy found that, for every 1 °C increase in bottom temperature, lobster carapace size at maturity decreased by 2.8 mm (Le Bris et al. 2017). Moreover, lobster are more susceptible to epizootic shell disease at temperatures above 10 °C and this condition can be fatal above 15 °C (Stewart 1980). As well as reducing their survival, the signs of this disease can reduce catch value due to the presence of the characteristic corrosive brown-black lesions on lobster carapaces (Glenn and Pugh 2006; Castro et al. 2012). The prevalence of epizootic shell disease is strongly correlated with temperature and is, consequently, currently more of a concern in southern New England than in the Gulf of Maine and Scotian Shelf (Shields 2019; Mazur et al. 2020). As temperatures continue to warm in the Northwest Atlantic (Wang et al. 2018), epizootic shell disease could potentially spread further north into Nova Scotia (Maynard et al. 2016; Groner et al. 2018; Greenan et al. 2019). Consequently, further studies are warranted on the potential effects of epizootic shell disease on thermal tolerance, i.e., do additional stressors such as shell disease affect thermal maximum?
Live lobster from Atlantic Canada is a high-value product (Fisheries and Oceans Canada 2022) that is shipped around the globe using artificial cooling and oxygenation that comprises a substantial part of the international seafood market (Fotedar and Evans 2011). Despite best practices to ensure lobster survival, many international lobster shipments arrive with some deceased lobster (Leo Muise, Executive Director—Nova Scotia Seafood Alliance pers. comm., 2020). The sale of dead lobster is illegal in Nova Scotia under the Fish Inspection Regulations and harvesters and lobster pound operators can face a substantial fine if they are caught in violation this (Province of Nova Scotia 2017). These regulations are unique to Canada. For example, lobster harvesters in the United States are permitted to process and sell dead lobster, while Norway lobster (Nephrops norvegicus) landed in Belgian harbors can be sold as lobster tails with the heads having been discarded in transit from the catch site (Bekaert et al. 2015). The application of PPG as described in the present study could be used to monitor signs of stress (e.g., arrythmia) in American lobster prior to international shipment to potentially identify weak animals, ultimately reducing mortality rates during transportation.
In spite of the unique challenges that will be brought on by climate change within individual LFAs (Brickman et al. 2021), acclimation temperature was the only significant predictor of euthanasia temperature in American lobster in the present study. This study demonstrates that adult American lobster living in the relatively cold waters surrounding Nova Scotia (Wang et al. 2018) can acclimate to new temperatures as ocean temperatures continue to rise, up to a certain point. Additional studies on other American lobster life stages would be required to assess their acclimation and thermal tolerances. Using heart rate data loggers (Gutzler and Watson 2022) for long-term deployment on lobster populations in the wild in Nova Scotia would provide additional valuable information on the effects of climate change on heart rate. Additionally, further research investigating the potential effects of thermal acclimation on survivability of soft-shelled lobster is warranted as global ocean temperatures continue to rise and adversely impact the lobster fishing industry.
Acknowledgements
The authors would like to thank Julia Skinner and Karetta Simmons for their assistance with experimentation, Paul MacIsaac for his assistance with animal husbandry, and Christopher Ferguson for his assistance with three-dimensional sketching. The authors would like to thank the anonymous reviewers for their constructive commentary on this manuscript. Funding for this work was provided by Atlantic Fisheries Fund AFF-NS-1605 and NSERC RGPIN-2018-05894.
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Published In
FACETS
Volume 9 • Number 1 • January 2024
Pages: 1 - 9
Editor: Mark D. Fast
History
Received: 11 October 2023
Accepted: 26 March 2024
Version of record online: 8 August 2024
Notes
This paper is part of a collection entitled One Ocean Health.
Copyright
© 2024 The Author(s). This work is licensed under a Creative Commons Attribution 4.0 International License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author(s) and source are credited.
Data Availability Statement
Data generated or analyzed during this study are available from the corresponding author upon reasonable request.
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Author Contributions
Conceptualization: RAH, KFC, LML, GKR
Formal analysis: RAH
Funding acquisition: RAH, LML, GKR
Investigation: RAH, KLW
Methodology: RAH, KFC
Project administration: KLW, LML
Resources: KFC, LML
Software: RAH, KFC
Supervision: GKR
Writing – original draft: RAH
Writing – review & editing: RAH, KFC, KLW, LML, GKR
Competing Interests
The authors declare there are no competing interests.
Funding Information
Atlantic Fisheries Fund: AFF-NS-1605
Natural Sciences and Engineering Research Council of Canada: RGPIN-2018-05894
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Ryan A. Horricks, K. Fraser Clark, Kiersten L. Watson, Leah M. Lewis-McCrea, and Gregor K. Reid. 2024. Effect of acclimation temperature on thermal tolerance between American lobster (Homarus americanus) collected in different lobster fishing areas in Atlantic Canada. FACETS.
9(): 1-9. https://doi.org/10.1139/facets-2023-0177
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