Plasticity of upper thermal limits of Australian Paratya spp. (Decapoda, Atyidae) and considerations of climate-change adaptation
Brendan Cox
A * , Amanda Reichelt-Brushett A , Kathryn Taffs A B and Ross Smith A C
+ Author Affiliations
- Author Affiliations
A Faculty of Science and Engineering, Southern Cross University, Lismore, NSW, Australia.
B NSW Department of Planning and Environment, Water Science, Ballina, NSW, Australia.
C Hydrobiology Pty Ltd, Brisbane, Qld, Australia.
Marine and Freshwater Research 74(6) 491-499 https://doi.org/10.1071/MF22260
Submitted: 1 December 2022 Accepted: 14 February 2023 Published: 14 March 2023
© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)
Abstract
Context: The ability of ectothermic stream invertebrates to adapt to the predicted increases in mean and extreme stream temperatures is crucial to ensuring they continue to exist.
Aims: To examine the plasticity of thermal limits of Australian Paratya spp. (Decapoda, Atyidae) from streams in eastern New South Wales (NSW). We hypothesised that the upper lethal temperature (ULT, as indicated by the median lethal temperature, LT50) would be higher for warm water-acclimated shrimp individuals than for winter-acclimatised shrimp individuals because of the importance of acclimatisation temperature.
Methods: Controlled experiments were undertaken to determine the ULT by using ramping assays for winter field-acclimatised and warm water laboratory-acclimated Paratya spp.
Key results: Warm water-acclimated shrimp individuals demonstrated a significantly higher LT50 of 36.1°C than did winter-acclimatised shrimp individuals at 34.6°C. Paratya spp. exhibited a limited plasticity for acclimation to warmer temperatures.
Conclusions: Results demonstrated the potential vulnerability of ectothermic stream invertebrates to climate change if stream temperatures increase as predicted and thermal thresholds are exceeded.
Implications: Understanding the ULT of stream invertebrates helps predict their ability to respond to temperature variability and response to climate change. Increasing resilience through target management of resorting riparian vegetation for shade and securing environmental flows may reduce the impacts of stream warming.
Keywords: acclimatisation, climate change, distribution, macroinvertebrates, plasticity, shrimp, stream temperature, thermal tolerance.
References
Alba-Tercedor, J, Sáinz-Bariáin, M, Poquet, JM, and Rodríguez-López, R (2017). Predicting river macroinvertebrate communities distributional shifts under future global change scenarios in the Spanish mediterranean area. PLoS ONE 12, e0167904.| Predicting river macroinvertebrate communities distributional shifts under future global change scenarios in the Spanish mediterranean area.Crossref | GoogleScholarGoogle Scholar |
Amundrud, SL, and Srivastava, DS (2020). Thermal tolerances and species interactions determine the elevational distributions of insects. Global Ecology and Biogeography 29, 1315–1327.
| Thermal tolerances and species interactions determine the elevational distributions of insects.Crossref | GoogleScholarGoogle Scholar |
Archambault, JM, Cope, WG, and Kwak, TJ (2014). Survival and behaviour of juvenile unionid mussels exposed to thermal stress and dewatering in the presence of a sediment temperature gradient. Freshwater Biology 59, 601–613.
| Survival and behaviour of juvenile unionid mussels exposed to thermal stress and dewatering in the presence of a sediment temperature gradient.Crossref | GoogleScholarGoogle Scholar |
Arias Font, R, Khamis, K, Milner, AM, Sambrook Smith, GH, and Ledger, ME (2021). Low flow and heatwaves alter ecosystem functioning in a stream mesocosm experiment. Science of The Total Environment 777, 146067.
| Low flow and heatwaves alter ecosystem functioning in a stream mesocosm experiment.Crossref | GoogleScholarGoogle Scholar |
Bain, PA, Gregg, AL, and Kumar, A (2016). De novo assembly and analysis of changes in the protein-coding transcriptome of the freshwater shrimp Paratya australiensis (Decapoda: Atyidae) in response to acid sulfate drainage water. BMC Genomics 17, 890.
| De novo assembly and analysis of changes in the protein-coding transcriptome of the freshwater shrimp Paratya australiensis (Decapoda: Atyidae) in response to acid sulfate drainage water.Crossref | GoogleScholarGoogle Scholar |
Bonacina, L, Fasano, F, Mezzanotte, V, and Fornaroli, R (2023). Effects of water temperature on freshwater macroinvertebrates: a systematic review. Biological Reviews 98, 191–221.
| Effects of water temperature on freshwater macroinvertebrates: a systematic review.Crossref | GoogleScholarGoogle Scholar |
Bruno, D, Belmar, O, Maire, A, Morel, A, Dumont, B, and Datry, T (2019). Structural and functional responses of invertebrate communities to climate change and flow regulation in alpine catchments. Global Change Biology 25, 1612–1628.
| Structural and functional responses of invertebrate communities to climate change and flow regulation in alpine catchments.Crossref | GoogleScholarGoogle Scholar |
Chessman, BC (2009). Climatic changes and 13-year trends in stream macroinvertebrate assemblages in New South Wales, Australia. Global Change Biology 15, 2791–2802.
| Climatic changes and 13-year trends in stream macroinvertebrate assemblages in New South Wales, Australia.Crossref | GoogleScholarGoogle Scholar |
Chessman, BC (2018). Dissolved-oxygen, current and temperature preferences of stream invertebrates estimated from field distributions: application to assemblage responses to drought. Hydrobiologia 809, 141–153.
| Dissolved-oxygen, current and temperature preferences of stream invertebrates estimated from field distributions: application to assemblage responses to drought.Crossref | GoogleScholarGoogle Scholar |
Cook, BD, Baker, AM, Page, TJ, Grant, SC, Fawcett, JH, Hurwood, DA, and Hughes, JM (2006). Biogeographic history of an Australian freshwater shrimp, Paratya australiensis (Atyidae): the role life history transition in phylogeographic diversification. Molecular Ecology 15, 1083–1093.
| Biogeographic history of an Australian freshwater shrimp, Paratya australiensis (Atyidae): the role life history transition in phylogeographic diversification.Crossref | GoogleScholarGoogle Scholar |
Cox, TJ, and Rutherford, JC (2000). Predicting the effects of time-varying temperatures on stream invertebrate mortality. New Zealand Journal of Marine and Freshwater Research 34, 209–215.
| Predicting the effects of time-varying temperatures on stream invertebrate mortality.Crossref | GoogleScholarGoogle Scholar |
CSIRO and Bureau of Meteorology (2020) State of the climate 2022. (Australian Government: Canberra, ACT, Australia) Available at http://www.bom.gov.au/state-of-the-climate/2022/documents/2022-state-of-the-climate-web.pdf
Dallas, HF, and Ketley, ZA (2011). Upper thermal limits of aquatic macroinvertebrates: comparing critical thermal maxima with 96-LT50 values. Journal of Thermal Biology 36, 322–327.
| Upper thermal limits of aquatic macroinvertebrates: comparing critical thermal maxima with 96-LT50 values.Crossref | GoogleScholarGoogle Scholar |
Dallas, HF, and Rivers-Moore, NA (2018). Temporal thermal refugia and seasonal variation in upper thermal limits of two species of riverine invertebrates: the amphipod, Paramelita nigroculus, and the mayfly, Lestagella penicillata. Aquatic Ecology 52, 333–349.
| Temporal thermal refugia and seasonal variation in upper thermal limits of two species of riverine invertebrates: the amphipod, Paramelita nigroculus, and the mayfly, Lestagella penicillata.Crossref | GoogleScholarGoogle Scholar |
Dudgeon, D (2019). Multiple threats imperil freshwater biodiversity in the anthropocene. Current Biology 29, R960–R967.
| Multiple threats imperil freshwater biodiversity in the anthropocene.Crossref | GoogleScholarGoogle Scholar |
Egea-Serrano, A, Alves, MC, Solé, M, and Tejedo, M (2022). Upper thermal tolerances and vulnerability to global warming in a Brazilian Caatinga fish Astyanax bimaculatus (Linnaeus, 1758) population. Austral Ecology 47, 1157–1161.
| Upper thermal tolerances and vulnerability to global warming in a Brazilian Caatinga fish Astyanax bimaculatus (Linnaeus, 1758) population.Crossref | GoogleScholarGoogle Scholar |
Ernst, MR, Beitinger, TL, and Stewart, KW (1984). Critical thermal maxima of nymphs of three Plecoptera species from an Ozark foothill stream. Freshwater Invertebrate Biology 3, 80–85.
| Critical thermal maxima of nymphs of three Plecoptera species from an Ozark foothill stream.Crossref | GoogleScholarGoogle Scholar |
Fenoglio, S, Bo, T, Cucco, M, Mercalli, L, and Malacarne, G (2010). Effects of global climate change on freshwater biota: a review with special emphasis on the Italian situation. Italian Journal of Zoology 77, 374–383.
| Effects of global climate change on freshwater biota: a review with special emphasis on the Italian situation.Crossref | GoogleScholarGoogle Scholar |
Ferris, R, and Wilson, RS (2012). The physiological arms race: exploring thermal acclimation among interacting species. Journal of Thermal Biology 37, 236–242.
| The physiological arms race: exploring thermal acclimation among interacting species.Crossref | GoogleScholarGoogle Scholar |
Fuller, MR, Leinenbach, P, Detenbeck, NE, Labiosa, R, and Isaak, DJ (2022). Riparian vegetation shade restoration and loss effects on recent and future stream temperatures. Restoration Ecology 30, e13626.
| Riparian vegetation shade restoration and loss effects on recent and future stream temperatures.Crossref | GoogleScholarGoogle Scholar |
Gomez Isaza, DF, Cramp, RL, and Franklin, CE (2022). Fire and rain: a systematic review of the impacts of wildfire and associated runoff on aquatic fauna. Global Change Biology 28, 2578–2595.
| Fire and rain: a systematic review of the impacts of wildfire and associated runoff on aquatic fauna.Crossref | GoogleScholarGoogle Scholar |
González, RA, Díaz, F, Licea, A, Denisse Re, A, Noemí Sánchez, L, and García-Esquivel, Z (2010). Thermal preference, tolerance and oxygen consumption of adult white shrimp Litopenaeus vannamei (Boone) exposed to different acclimation temperatures. Journal of Thermal Biology 35, 218–224.
| Thermal preference, tolerance and oxygen consumption of adult white shrimp Litopenaeus vannamei (Boone) exposed to different acclimation temperatures.Crossref | GoogleScholarGoogle Scholar |
Gunderson, AR, and Stillman, JH (2015). Plasticity in thermal tolerance has limited potential to buffer ectotherms from global warming. Proceedings of the Royal Society of London – B. Biological Sciences 282, 20150401.
Haase, P, Pilotto, F, Li, F, Sundermann, A, Lorenz, AW, Tonkin, JD, and Stoll, S (2019). Moderate warming over the past 25 years has already reorganized stream invertebrate communities. Science of The Total Environment 658, 1531–1538.
| Moderate warming over the past 25 years has already reorganized stream invertebrate communities.Crossref | GoogleScholarGoogle Scholar |
Hancock, MA, and Bunn, SE (1997). Population dynamics and life history of Paratya australiensis Kemp, 1917 (Decapoda: Atyidae) in upland rainforest streams, south-eastern Queensland, Australia. Marine and Freshwater Research 48, 361.
| Population dynamics and life history of Paratya australiensis Kemp, 1917 (Decapoda: Atyidae) in upland rainforest streams, south-eastern Queensland, Australia.Crossref | GoogleScholarGoogle Scholar |
Hidalgo-Galiana, A, Ribera, I, and Terblanche, JS (2021). Geographic variation in acclimation responses of thermal tolerance in South African diving beetles (Dytiscidae: Coleoptera). Comparative Biochemistry and Physiology – A. Molecular & Integrative Physiology 257, 110955.
| Geographic variation in acclimation responses of thermal tolerance in South African diving beetles (Dytiscidae: Coleoptera).Crossref | GoogleScholarGoogle Scholar |
Houghton, DC, and Shoup, L (2014). Seasonal changes in the critical thermal maxima of four species of aquatic insects (Ephemeroptera, Trichoptera). Environmental Entomology , 1059–1066.
| Seasonal changes in the critical thermal maxima of four species of aquatic insects (Ephemeroptera, Trichoptera).Crossref | GoogleScholarGoogle Scholar |
Isaak, DJ, Wollrab, S, Horan, D, and Chandler, G (2012). Climate change effects on stream and river temperatures across the northwest US. From 1980–2009 and implications for salmonid fishes. Climatic Change 113, 499–524.
| Climate change effects on stream and river temperatures across the northwest US. From 1980–2009 and implications for salmonid fishes.Crossref | GoogleScholarGoogle Scholar |
Johnson, SL (2004). Factors influencing stream temperatures in small streams: substrate effects and a shading experiment. Canadian Journal of Fisheries and Aquatic Sciences 61, 913–923.
| Factors influencing stream temperatures in small streams: substrate effects and a shading experiment.Crossref | GoogleScholarGoogle Scholar |
Jørgensen, LB, Malte, H, and Overgaard, J (2019). How to asses Drosophila heat tolerance: unifying static and dynamic tolerance assays to predict heat distribution limits. Functional Ecology 33, 629–642.
| How to asses Drosophila heat tolerance: unifying static and dynamic tolerance assays to predict heat distribution limits.Crossref | GoogleScholarGoogle Scholar |
Kim, KS, Chou, H, Funk, DH, Jackson, JK, Sweeney, BW, and Buchwalter, DB (2017). Physiological responses to short-term thermal stress in mayfly (Neocloeon triangulifer) larvae in relation to upper thermal limits. Journal of Experimental Biology 220, 2598–2605.
| Physiological responses to short-term thermal stress in mayfly (Neocloeon triangulifer) larvae in relation to upper thermal limits.Crossref | GoogleScholarGoogle Scholar |
Magozzi, S, and Calosi, P (2015). Integrating metabolic performance, thermal tolerance, and plasticity enables for more accurate predictions on species vulnerability to acute and chronic effects of global warming. Global Change Biology 21, 181–194.
| Integrating metabolic performance, thermal tolerance, and plasticity enables for more accurate predictions on species vulnerability to acute and chronic effects of global warming.Crossref | GoogleScholarGoogle Scholar |
Morley, SA, Peck, LS, Sunday, JM, Heiser, S, and Bates, AE (2019). Physiological acclimation and persistence of ectothermic species under extreme heat events. Global Ecology and Biogeography 28, 1018–1037.
| Physiological acclimation and persistence of ectothermic species under extreme heat events.Crossref | GoogleScholarGoogle Scholar |
Moulton, TP, Souza, ML, Brito, EF, Braga, MRA, and Bunn, SE (2012). Strong interactions of Paratya australiensis (Decapoda: Atyidae) on periphyton in an Australian subtropical stream. Marine and Freshwater Research 63, 834.
| Strong interactions of Paratya australiensis (Decapoda: Atyidae) on periphyton in an Australian subtropical stream.Crossref | GoogleScholarGoogle Scholar |
Narum, SR, Campbell, NR, Meyer, KA, Miller, MR, and Hardy, RW (2013). Thermal adaptation and acclimation of ectotherms from differing aquatic climates. Molecular Ecology 22, 3090–3097.
| Thermal adaptation and acclimation of ectotherms from differing aquatic climates.Crossref | GoogleScholarGoogle Scholar |
Overgaard, J, Kristensen, TN, and Sørensen, JG (2012). Validity of thermal ramping assays used to assess thermal tolerance in arthropods. PLoS ONE 7, e32758.
| Validity of thermal ramping assays used to assess thermal tolerance in arthropods.Crossref | GoogleScholarGoogle Scholar |
Pallarés, S, Verberk, WCEP, and Bilton, DT (2021). Plasticity of thermal performance curves in a narrow range endemic water beetle. Journal of Thermal Biology 102, 103113.
| Plasticity of thermal performance curves in a narrow range endemic water beetle.Crossref | GoogleScholarGoogle Scholar |
Palmer, MA, Lettenmaier, DP, Poff, NL, Postel, SL, Richter, B, and Warner, R (2009). Climate change and river ecosystems: protection and adaptation options. Environmental Management 44, 1053–1068.
| Climate change and river ecosystems: protection and adaptation options.Crossref | GoogleScholarGoogle Scholar |
Pedreros, P, Guevara-Mora, M, Stehr, A, Araneda, A, and Urrutia, R (2020). Response of macroinvertebrate communities to thermal regime in small Mediterranean streams (southern South America): implications of global warming. Limnologica 81, 125763.
| Response of macroinvertebrate communities to thermal regime in small Mediterranean streams (southern South America): implications of global warming.Crossref | GoogleScholarGoogle Scholar |
Quinn, JM, Steele, GL, Hickey, CW, and Vickers, ML (1994). Upper thermal tolerances of twelve New Zealand stream invertebrate species. New Zealand Journal of Marine and Freshwater Research 28, 391–397.
| Upper thermal tolerances of twelve New Zealand stream invertebrate species.Crossref | GoogleScholarGoogle Scholar |
Rahman, S, Schmidt, D, and Hughes, JM (2020). Genetic structure of Australian glass shrimp, Paratya australiensis, in relation to altitude. PeerJ 8, e8139–e8139.
| Genetic structure of Australian glass shrimp, Paratya australiensis, in relation to altitude.Crossref | GoogleScholarGoogle Scholar |
Rezende, EL, Castañeda, LE, and Santos, M (2014). Tolerance landscapes in thermal ecology. Functional Ecology 28, 799–809.
| Tolerance landscapes in thermal ecology.Crossref | GoogleScholarGoogle Scholar |
Rivers-Moore, NA, Dallas, HF, and Ross-Gillespie, V (2013). Life history does matter in assessing potential ecological impacts of thermal changes on aquatic macroinvertebrates. River Research and Applications 29, 1100–1109.
| Life history does matter in assessing potential ecological impacts of thermal changes on aquatic macroinvertebrates.Crossref | GoogleScholarGoogle Scholar |
Rohr, JR, Civitello, DJ, Cohen, JM, Roznik, EA, Sinervo, B, and Dell, AI (2018). The complex drivers of thermal acclimation and breadth in ectotherms. Ecology Letters 21, 1425–1439.
| The complex drivers of thermal acclimation and breadth in ectotherms.Crossref | GoogleScholarGoogle Scholar |
Ross-Gillespie V (2014) Effects of water temperature on life-history traits of selected South African aquatic insects. PhD thesis, University of Cape Town, Cape Town, South Africa.
Semsar-kazerouni, M, and Verberk, WCEP (2018). It’s about time: linkages between heat tolerance, thermal acclimation and metabolic rate at different temporal scales in the freshwater amphipod Gammarus fossarum Koch, 1836. Journal of Thermal Biology 75, 31–37.
| It’s about time: linkages between heat tolerance, thermal acclimation and metabolic rate at different temporal scales in the freshwater amphipod Gammarus fossarum Koch, 1836.Crossref | GoogleScholarGoogle Scholar |
Seyedhashemi, H, Vidal, J-P, Diamond, JS, Thiéry, D, Monteil, C, Hendrickx, F, Maire, A, and Moatar, F (2022). Regional, multi-decadal analysis on the Loire River Basin reveals that stream temperature increases faster than air temperature. Hydrology and Earth System Sciences 26, 2583–2603.
| Regional, multi-decadal analysis on the Loire River Basin reveals that stream temperature increases faster than air temperature.Crossref | GoogleScholarGoogle Scholar |
Stewart, BA, Close, PG, Cook, PA, and Davies, PM (2013). Upper thermal tolerances of key taxonomic groups of stream invertebrates. Hydrobiologia 718, 131–140.
| Upper thermal tolerances of key taxonomic groups of stream invertebrates.Crossref | GoogleScholarGoogle Scholar |
Suter, PJ, Mynott, JH, and Crump, M (2022). New species of Paratya (Decapoda: Atyidae) from Australian inland waters – linking morphological characters with molecular lineages. Memoirs of Museum Victoria 81, 55–122.
| New species of Paratya (Decapoda: Atyidae) from Australian inland waters – linking morphological characters with molecular lineages.Crossref | GoogleScholarGoogle Scholar |
Sweeney BW, Jackson JK, Newbold JD, Funk DH (1992) Climate change and the life histories and biogeography of aquatic insects in eastern North America. In ‘Global climate change and freshwater ecosystems’. (Eds P Firth, SG Fisher) pp. 143–176. (Springer)
Terblanche, JS, and Hoffmann, AA (2020). Validating measurements of acclimation for climate change adaptation. Current Opinion in Insect Science 41, 7–16.
| Validating measurements of acclimation for climate change adaptation.Crossref | GoogleScholarGoogle Scholar |
Trimmel, H, Weihs, P, Leidinger, D, Formayer, H, Kalny, G, and Melcher, A (2018). Can riparian vegetation shade mitigate the expected rise in stream temperatures due to climate change during heat waves in a human-impacted pre-alpine river? Hydrology and Earth System Sciences 22, 437–461.
| Can riparian vegetation shade mitigate the expected rise in stream temperatures due to climate change during heat waves in a human-impacted pre-alpine river?Crossref | GoogleScholarGoogle Scholar |
Verberk, WCEP, and Calosi, P (2012). Oxygen limits heat tolerance and drives heat hardening in the aquatic nymphs of the gill breathing damselfly Calopteryx virgo (Linnaeus, 1758). Journal of Thermal Biology 37, 224–229.
| Oxygen limits heat tolerance and drives heat hardening in the aquatic nymphs of the gill breathing damselfly Calopteryx virgo (Linnaeus, 1758).Crossref | GoogleScholarGoogle Scholar |
Verberk, WCEP, Overgaard, J, Ern, R, Bayley, M, Wang, T, Boardman, L, and Terblanche, JS (2016). Does oxygen limit thermal tolerance in arthropods? A critical review of current evidence. Comparative Biochemistry and Physiology – A. Molecular & Integrative Physiology 192, 64–78.
| Does oxygen limit thermal tolerance in arthropods? A critical review of current evidence.Crossref | GoogleScholarGoogle Scholar |
Verberk, WCEP, Buchwalter, DB, and Kefford, BJ (2020). Energetics as a lens to understanding aquatic insect’s responses to changing temperature, dissolved oxygen and salinity regimes. Current Opinion in Insect Science 41, 46–53.
| Energetics as a lens to understanding aquatic insect’s responses to changing temperature, dissolved oxygen and salinity regimes.Crossref | GoogleScholarGoogle Scholar |
Verdelhos, T, Marques, JC, and Anastácio, P (2015). Behavioral and mortality responses of the bivalves Scrobicularia plana and Cerastoderma edule to temperature, as indicator of climate change’s potential impacts. Ecological Indicators 58, 95–103.
| Behavioral and mortality responses of the bivalves Scrobicularia plana and Cerastoderma edule to temperature, as indicator of climate change’s potential impacts.Crossref | GoogleScholarGoogle Scholar |
Ward, JV, and Stanford, JA (1982). Thermal responses in the evolutionary ecology of aquatic insects. Annual review of entomology 27, 97–117.
| Thermal responses in the evolutionary ecology of aquatic insects.Crossref | GoogleScholarGoogle Scholar |
Williams, W (1977). Some aspects of the ecology of Paratya australiensis (Crustacea: Decapoda: Atyidae). Marine and Freshwater Research 28, 403–415.
| Some aspects of the ecology of Paratya australiensis (Crustacea: Decapoda: Atyidae).Crossref | GoogleScholarGoogle Scholar |
