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Carbon dioxide enrichment alters predator avoidance and sex determination but only sex is mediated by GABAA receptors

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Abstract

We hypothesized that near-future elevated CO2 would affect the antipredatory behavior of two freshwater organisms; a pulmonate gastropod (Physella columbiana) and a cladoceran crustacean (Daphnia magna). Studies have found that pCO2 and increased acidification due to CO2 impedes fright responses to predators by activating GABAA receptors. After administration of predator-derived kairomones and conspecific alarm cues, we also briefly exposed some of the animals to gabazine which is a GABAA receptor antagonist to restore a fright response. We found that added carbon dioxide negatively affected the antipredatory behavior of both species but gabazine did not reverse this effect. To further examine the effect of CO2 and gabazine, we also tested the effect of stressful crowding, cold, and acidic conditions on the production of male daphnid offspring. An increase in ratio of male to female offspring is a common and expected response to stress by daphnids. We found that stress increased the production of males and gabazine reversed this at a pH of 5.5 but not at pH 6.2 or 6.5. Our study suggest that while the main negative effects of anthropogenic CO2 enrichment can be robust, the myriad indirect effects of CO2 make predictions about future predator prey systems less clear.

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References

  • Allan, B. J., P. Domenici, M. I. McCormick, S. A. Watson & P. L. Munday, 2013. Elevated CO2 affects predator-prey interactions through altered performance. PLoS ONE 8: e58520.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Atema, J. & D. Stenzler, 1977. Alarm substance of the marine mud snail, Nassarius obsoletus: Biological characterization and possible evolution. Journal of Chemical Ecology 3: 173–187.

    Google Scholar 

  • Barnhart, C. M., 1992. Acid-base regulation in pulmonate molluscs. Journal of Experimental Zoology 263: 120–126.

    CAS  Google Scholar 

  • Barry, M. J., 1998. Endosulfan-enhanced crest induction in Daphnia longicephala: evidence for cholinergic innervation of kairomone receptors. Journal of Plankton Research 20: 1219–1231.

    CAS  Google Scholar 

  • Belivermiş, M., M. Warnau, M. Metian, F. Oberhänsli, J. L. Teyssié & T. Lacoue-Labarthe, 2016. Limited effects of increased CO2 and temperature on metal and radionuclide bioaccumulation in a sessile invertebrate, the oyster Crassostrea gigas. ICES Journal of Marine Science 73: 753–763.

    Google Scholar 

  • Benson, J. A., 1989. A novel GABA receptor in the heart of a primitive arthropod, Limulus polyphemus. Journal of Experimental Biology 147: 421–438.

    CAS  Google Scholar 

  • Brauner, C. J. & D. W. Baker, 2009. Patterns of acid–base regulation during exposure to hypercarbia in fishes. In Glass, M. & S. Wood (eds), Cardio-respiratory control in vertebrates. Springer, Berlin, Heidelberg: 43–63.

    Google Scholar 

  • Browman, H. I., 2016. Applying organized scepticism to ocean acidification research. ICES Journal of Marine Science 73: 529–536.

    Google Scholar 

  • Briffa, M., K. de la Haye & P. L. Munday, 2012. High CO2 and marine animal behaviour: potential mechanisms and ecological consequences. Marine Pollution Bulletin 64: 1519–1528.

    CAS  PubMed  Google Scholar 

  • Cao, Z., F. Mu, X. Wei & Y. Sun, 2015. Influence of CO2-induced seawater acidification on the development and lifetime reproduction of Tigriopus japonicus Mori, 1938. Journal of Natural History 49: 2813–2826.

    Google Scholar 

  • Calosi, P., D. T. Bilton & J. I. Spicer, 2007. The diving response of a diving beetle: effects of temperature and acidification. Journal of Zoology 273: 289–297.

    Google Scholar 

  • Chevalier, J., E. Harscoët, M. Keller, P. Pandard, J. Cachot & M. Grote, 2015. Exploration of Daphnia behavioral effect profiles induced by a broad range of toxicants with different modes of action. Environmental Toxicology and Chemistry 34: 1760–1769.

    CAS  PubMed  Google Scholar 

  • Chivers, D., M. McCormick, G. Nilsson, P. Munday, S. Watson, M. Meekan, M. Mitchell, K. Corkill & M. Ferrari, 2014. Impaired learning of predators and lower prey survival under elevated CO2: a consequence of neurotransmitter interference. Global Change Biology 20: 515–522.

    PubMed  Google Scholar 

  • Chopelet, J., P. U. Blier & F. Dufresne, 2008. Plasticity of growth rate and metabolism in Daphnia magna populations from different thermal habitats. Journal of Experimental Zoology Part A: Ecological Genetics and Physiology 309: 553–562.

    CAS  Google Scholar 

  • Chung, W. S., N. J. Marshall, S. A. Watson, P. L. Munday & G. E. Nilsson, 2014. Ocean acidification slows retinal function in a damselfish through interference with GABAA receptors. The Journal of Experimental Biology 217: 323–326.

    CAS  PubMed  Google Scholar 

  • Cole, J. J., Y. T. Prairie, N. F. Caraco, W. H. McDowell, L. J. Tranvik, R. G. Striegl, C. M. Duarte, P. Kortelainen, J. A. Downing, J. Middleburg & J. Melack, 2007. Plumbing the global carbon cycle: integrating inland waters into the terrestrial carbon budget. Ecosystems 10: 171–184.

    CAS  Google Scholar 

  • Covich, A. P., M. A. Palmer & T. A. Crowl, 1999. The role of benthic invertebrate species in freshwater ecosystems: zoobenthic species influence energy flows and nutrient cycling. Bioscience 49: 119–127.

    Google Scholar 

  • Crossno, S. K., L. H. Kalbus & G. E. Kalbus, 1996. Determinations of carbon dioxide by titration. Journal of Chemical Education 73: 175–176.

    CAS  Google Scholar 

  • DeMille, C., S. Arnott & G. Pyle, 2016. Variation in copper effects on kairomone-mediated responses in Daphnia pulicaria. Ecotoxicology and Environmental Safety 126: 264–272.

    CAS  PubMed  Google Scholar 

  • Dickey, B. F. & T. M. McCarthy, 2007. Predator and prey interactions between crayfish (Orconectes juvenilis) and snails (Physa gyrina) are affected by spatial scale and chemical cues. Invertebrate Biology 126: 57–66.

    Google Scholar 

  • Engelbrecht, W., O. Hesse, J. Wolinska & C. Laforsch, 2013. Two threats at once: encounters with predator cues alter host life-history and morphological responses to parasite spores. Hydrobiologia 715: 93–100.

    Google Scholar 

  • Esbaugh, A. J., R. Heuer & M. Grosell, 2012. Impacts of ocean acidification on respiratory gas exchange and acid–base balance in a marine teleost, Opsanus beta. Journal of Comparative Physiology B 182: 921–934.

    CAS  Google Scholar 

  • Feely, R. A., S. C. Doney & S. R. Cooley, 2009. Ocean acidification: present conditions and future changes in a high-CO2 world. Oceanography 22: 36–47.

    Google Scholar 

  • Ferrari, M., M. McCormick, P. Munday, M. Meekan, D. Dixson, O. Lonnstedt & D. Chivers, 2011. Putting prey and predator into the CO2 equation—qualitative and quantitative effects of ocean acidification on predator–prey interactions. Ecology Letters 14: 1143–1148.

    PubMed  Google Scholar 

  • Gattuso, J. P., K. Gao, K. Lee, B. Rost & K. G. Schulz, 2010. Approaches and tools to manipulate the carbonate chemistry. In Riebesell, U., V. J. Fabry, L. Hansson & J. P. Gattuso (eds), Guide to best practices for ocean acidification research and data reporting. European Union, Luxembourg: 41–52.

    Google Scholar 

  • Haapala, H., P. Sepponen & E. Meskus, 1975. Effect of Spring floods on water acidity in the Kiiminkijoki Area, Finland. Oikos 26: 26–31.

    CAS  Google Scholar 

  • Hamilton, T. J., A. Holcombe & M. Tresguerres, 2014. CO2-induced ocean acidification increases anxiety in Rockfish via alteration of GABAA receptor functioning. Proceedings of the Royal Society B 281: 20132509.

    PubMed  Google Scholar 

  • Hasler, C. T., D. Butman, J. D. Jeffrey & C. D. Suski, 2016. Freshwater biota and rising pCO2? Ecology Letters 19: 98–108.

    PubMed  Google Scholar 

  • Havens, K., J. Beaver, E. Manis & T. East, 2015. Inter-lake comparisons indicate that fish predation, rather than high temperature, is the major driver of summer decline in Daphnia and other changes among cladoceran zooplankton in subtropical Florida lakes. Hydrobiologia 750: 57–67.

    CAS  Google Scholar 

  • Henschel, O., K. E. Gipson & A. Bordey, 2008. GABAA receptors, anesthetics and anticonvulsants in brain development. CNS & Neurological Disorders-Drug Targets 7: 211–224.

    CAS  Google Scholar 

  • Herzog, Q., M. Rabus, B. Wolfschoon Ribeiro & C. Laforsch, 2016. Inducible defenses with a “twist”: Daphnia barbata abandons bilateral symmetry in response to an ancient predator. Plos ONE 11: 1–6.

    Google Scholar 

  • Holcombe, G. W., G. L. Phipps & J. W. Marier, 1984. Methods for conducting snail (Aplexa hypnorum) embryo through adult exposures: effects of cadmium and reduced pH levels. Archives of Environmental Contamination and Toxicology 13: 627–634.

    CAS  Google Scholar 

  • Ignace, D. D., S. I. Dodson & D. R. Kashian, 2011. Identification of the critical timing of sex determination in Daphnia magna (Crustacea, Branchiopoda) for use in toxicological studies. Hydrobiologia 668: 117–123.

    CAS  Google Scholar 

  • IPCC, 2014. Climate change 2014: synthesis report. In Pachauri, R. K., L. A. Meyer & Core Writing Team (eds), Contribution of working groups I, II and III to the fifth assessment report of the intergovernmental panel on climate change. IPCC, Geneva: 151.

    Google Scholar 

  • Kim, T. W., J. Taylor, C. Lovera & J. P. Barry, 2016. CO2-driven decrease in pH disrupts olfactory behaviour and increases individual variation in deep-sea hermit crabs. ICES Journal of Marine Science 73: 613–619.

    Google Scholar 

  • Kroeker, K. J., S. Sanford, B. M. Jellison & B. P. Gaylord, 2014. Predicting the effects of ocean acidification on predator-prey interactions: a conceptual framework based on coastal molluscs. Biological Bulletin 226: 211–222.

    PubMed  Google Scholar 

  • Isari, S., S. Zervoudake, E. Saiz, C. Pelejero & J. Peters, 2015. Copepod vital rates under CO2-induced acidification: a calanoid species and a cyclopoid species under short-term exposures. Journal of Plankton Research 37: 912–922.

    CAS  Google Scholar 

  • Jansen, M., C. Buser, R. Stoks, L. De Meester & A. Cielen, 2011. The interplay of past and current stress exposure on the water flea Daphnia. Functional Ecology 25: 974–982.

    Google Scholar 

  • Leduc, A. O. H. C., E. Roh, M. C. Harvey & G. E. Brown, 2006. Impaired detection of chemical alarm cues by juvenile wild Atlantic salmon (Salmo salar) in a weakly acidic environment. Canadian Journal of Fisheries and Aquatic Sciences 63: 2356–2363.

    Google Scholar 

  • Leduc, A. O. H. C., P. L. Munday, G. E. Brown & M. C. O. Ferrari, 2013. Effects of acidification on olfactory-mediated behaviour in freshwater and marine ecosystems: a synthesis. Philosophical Transactions of the Royal Society B: Biological Sciences 368: 20120447.

    Google Scholar 

  • Lefcort, F., K. Venstrom, J. A. McDonald & L. F. Reichardt, 1992. Regulation of expression of fibronectin and its receptor, alpha 5 beta 1, during development and regeneration of peripheral nerve. Development 116: 767–782.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lefcort, H., 1996. An adaptive, chemically mediated fright response in tadpoles of the southern leopard frog, Rana utricularia. Copeia 1996: 455–459.

    Google Scholar 

  • Lefcort, H. & B. P. Kotler, 2017. Life in a near-future atmosphere: carbon dioxide enrichment increases plant growth and alters the behavior of a terrestrial snail but not a terrestrial beetle. Israel Journal of Ecology and Evolution 63: 33–38.

    Google Scholar 

  • Lefcort, H., D. P. Abbott, D. A. Cleary, E. Howell, N. C. Keller & M. M. Smith, 2004. Aquatic snails from mining sites have evolved to detect and avoid heavy metals. Archives of Environmental Contamination and Toxicology 46: 478–484.

    CAS  PubMed  Google Scholar 

  • Lefcort, H., D. A. Cleary, A. M. Marble, M. V. Phillips, T. J. Stoddard, L. M. Tuthill & J. R. Winslow, 2015. Snails from heavy-metal polluted environments have reduced sensitivity to carbon dioxide-induced acidity. SpringerPlus 4: 1–9.

    CAS  Google Scholar 

  • Lewis, E., D. W. R. Wallace, & L. J. Allison, 1998. CO2SYS-Program developed for CO2 system calculations. https://www.researchgate.net/publication/240194526_CO2SYS-Program_developed_for_CO2_system_calculations.

  • Li, Y., W. X. Wang & M. Wang, 2017. Alleviation of mercury toxicity to a marine copepod under multigenerational exposure by ocean acidification. Scientific Reports 7: 324.

    PubMed  PubMed Central  Google Scholar 

  • Lippert, K. A., J. M. Gunn & G. E. Morgan, 2007. Effects of colonizing predators on yellow perch (Perca flavescens) populations in lakes recovering from acidification and metal stress. Canadian Journal of Fisheries and Aquatic Sciences 64: 1413–1428.

    CAS  Google Scholar 

  • Maberly, S. C., 1996. Diel, episodic and seasonal changes in pH and concentrations of inorganic carbon in a productive lake. Freshwater Biology 35: 579–598.

    CAS  Google Scholar 

  • Mason, B. J., 1992. Acid rain: its causes and its effects on inland waters. In Mason, B. J. (ed.), Science, technology, and, society series. Oxford University Press, Clarendon Press, Oxford, New York.

    Google Scholar 

  • Maud, C. O., M. I. Ferrari, S. A. McCormick, M. G. Meekan, P. L. Munday & D. P. Chivers, 2017. Predation in high CO2 waters: prey fish from high-risk environments are less susceptible to ocean acidification. Integrative and Comparative Biology 57: 55–62.

    Google Scholar 

  • McCarthy, M. M., A. M. Davis & J. A. Mong, 1996. Excitatory neurotransmission and sexual differentiation of the brain. Brain Research Bulletin 44: 487–495.

    Google Scholar 

  • McCoole, M. B., B. T. D’Andrea, K. N. Baer & A. E. Christie, 2012. Genomic analyses of gas (nitric oxide and carbon monoxide) and small molecule transmitter (acetylcholine, glutamate and GABA) signaling systems in Daphnia pulex. Comparative Biochemistry and Physiology Part D: Genomics and Proteomics 7: 124–160.

    CAS  Google Scholar 

  • McElhany, P., 2016. CO2 sensitivity experiments are not sufficient to show an effect of ocean acidification. ICES Journal of Marine Science 74: 926–928.

    Google Scholar 

  • McQueen, D. J., J. R. Post & E. L. Mills, 1986. Trophic Relationships in Freshwater Pelagic Ecosystems. Canadian Journal of Fisheries and Aquatic Sciences 43: 1571–1581.

    Google Scholar 

  • Miyakawa, H., N. Sugimoto, T. Kohyama, T. Iguchi & T. Miura, 2015. Intra-specific variations in reaction norms of predator-induced polyphenism in the water flea Daphnia pulex. Ecological Research 30: 705–713.

    Google Scholar 

  • Mirza, R. & G. Pyle, 2009. Waterborne metals impair inducible defenses in Daphnia pulex: morphology, life-history traits and encounters with predators. Freshwater Biology 54: 1016–1027.

    Google Scholar 

  • Munday, P., D. Dixson, M. McCormick, M. Meekan, M. Ferrari & D. Chivers, 2010. Replenishment of fish populations is threatened by ocean acidification. Proceedings National Academy Sciences United States of America 107: 12930–12934.

    CAS  Google Scholar 

  • Navarro, J. M., C. Duarte, P. H. Manríquez, M. A. Lardies, R. Torres, K. Acuña, C. A. Vargas & N. A. Lagos, 2016. Ocean warming and elevated carbon dioxide: multiple stressor impacts on juvenile mussels from southern Chile. ICES Journal of Marine Science 73: 710–764.

    Google Scholar 

  • Nilsson, G. E., D. L. Dixson, P. Domenici, M. I. McCormick, C. Sorensen, S. A. Watson & P. L. Munday, 2012. Near-future carbon dioxide levels alter fish behaviour by interfering with neurotransmitter function. Nature Climate Change 2: 201–204.

    CAS  Google Scholar 

  • O’Brien, C. & D. W. Blinn, 1999. The endemic spring snail Pyrgulopsis montezumensis in a high CO2 environment: importance of extreme chemical habitats as refugia. Freshwater Biology 42: 225–234.

    Google Scholar 

  • Okland, J. & K. A. Okland, 1986. The effects of acid deposition on benthic animals in lakes and streams. Experientia 42: 471–486.

    Google Scholar 

  • Ou, M., T. J. Hamilton, J. Eom, E. M. Lyall, J. Gallup, A. Jiang, J. Lee, D. A. Close, S. S. Yun & C. J. Brauner, 2015. Responses of pink salmon to CO2-induced aquatic acidification. Nature Climate Change 5: 950–955.

    CAS  Google Scholar 

  • Palma, P., V. L. Palma, R. M. Fernandes, A. M. V. M. Soares & I. R. Barbosa, 2009. Endosulfan sulphate interferes with reproduction, embryonic development and sex differentiation in Daphnia magna. Ecotoxicology and Environmental Safety 72: 344–350.

    CAS  PubMed  Google Scholar 

  • Pestana, J., A. Soares & D. Baird, 2013. Predator threat assessment in Daphnia magna: the role of kairomones versus conspecific alarm cues. Marine and Freshwater Research 64: 679–686.

    Google Scholar 

  • Phillips, J. C., G. A. McKinley, V. Bennington, H. A. Bootsma, D. J. Pilcher, R. W. Sterner & N. R. Urban, 2015. The potential for CO2-induced acidification in freshwater: a Great Lakes case study. Oceanography 28: 136–145.

    Google Scholar 

  • Pierobon, P., A. Tino, R. Minei & G. Marino, 2004. Different roles of GABA and glycine in the modulation of chemosensory responses in Hydra vulgaris (Cnidaria, Hydrozoa). Hydrobiologia 530(531): 59–66.

    Google Scholar 

  • Pijanowska, J. & A. Kowalczewski, 1997. Cues from injured Daphnia and from cyclopoids feeding on Daphnia can modify life histories of conspecifics. Hydrobiologia 350: 99–103.

    Google Scholar 

  • Raymond, P. A., J. Hartmann, R. Lauerwald, S. Sobek, C. McDonald, M. Hoover, D. Butman, R. Striegl, E. Mayorga, C. Humborg, P. Kortelainen, M. Meybeck, P. Ciai & P. Guth, 2013. Global carbon dioxide emissions from inland waters. Nature 503: 355–359.

    CAS  PubMed  Google Scholar 

  • Regan, M., A. Turko, J. Heras, M. Andersen, S. Lefevre, W. Tobias, M. Bayley, C. Brauner, H. Do Thi Than, P. Nguyen Thanh & G. Nilsson, 2016. Ambient CO2, fish behaviour and altered GABAergic neurotransmission: exploring the mechanism of CO2-altered behaviour by taking a hypercapnia dweller down to low CO2 levels. Journal of Experimental Biology 219: 109–118.

    PubMed  Google Scholar 

  • Reisert, I., K. Lieb, C. Beyer & C. Pilgrim, 1996. Sex differentiation of rat hippocampal GABAergic neurons. European Journal of Neuroscience 8: 1718–1724.

    CAS  PubMed  Google Scholar 

  • Roozen, F. & M. Lurling, 2001. Behavioural response of Daphnia to olfactory cues from food, competitors and predators. Journal Of Plankton Research 23: 797–808.

    Google Scholar 

  • Ross, P. M., L. Parker & M. Byrne, 2016. Transgenerational responses of molluscs and echinoderms to changing ocean conditions. ICES Journal of Marine Science 73: 537–549.

    Google Scholar 

  • Schram, J. B., K. M. Schoenrock, J. B. McClintock, C. D. Amsler & R. A. Angus, 2016. Testing Antarctic resilience: the effects of elevated seawater temperature and decreased pH on two gastropod species. ICES Journal of Marine Science 73: 739–752.

    Google Scholar 

  • Servos, M. R. & G. L. Mackie, 1986. The effect of short-term acidification during spring snowmelt on selected Mollusca in south-central Ontario. Canadian Journal of Zoology 64: 1690–1695.

    Google Scholar 

  • Sigel, E., 2002. Mapping of the benzodiazepine recognition site on GABAA receptors. Current Topics in Medicinal Chemistry 2: 833–869.

    CAS  PubMed  Google Scholar 

  • Staley, K. J., B. L. Soldo & W. R. Proctor, 1995. Ionic mechanisms of neuronal excitation by inhibitory GABAA receptors. Science 269: 977–981.

    CAS  PubMed  Google Scholar 

  • Stocker, T.F., D. Qin, G. K. Plattner, Tignor M. M. B., S. K. Allen, J. Boschung, A. Nauels, Y. Xia, V. Bex & P. M. Midgley, 2013. IPCC, 2013: Climate Change 2013: The Physical Science Basis. Working Group I Contribution to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change.

  • Strahl, J., D. S. Francis, J. Doyle, C. Humphrey & K. E. Fabricius, 2015. Biochemical responses to ocean acidification contrast between tropical corals with high and low abundances at volcanic carbon dioxide seeps. ICES Journal of Marine Science 73: 897–909.

    Google Scholar 

  • Tepper, J. M. & C. R. Lee, 2007. GABAergic control of substantia nigra dopaminergic neurons. Science Direct 160: 189–208.

    CAS  Google Scholar 

  • Tonkopiĭ, V., N. Podosinovikova, A. Zagrebin, L. Sherstneva, V. Petrov, L. Mukovskiĭ & V. Dolgo-Saburov, 2005. Daphnia magna Straus: a test object for the pharmacological evaluation of GABA-ergic drugs in the whole organism. Eksperimental’naia I Klinicheskaia Farmakologiia 68: 55–58.

    PubMed  Google Scholar 

  • Tresguerres, M. & T. J. Hamilton, 2017. Acid–base physiology, neurobiology and behaviour in relation to CO2-induced ocean acidification. Journal of Experimental Biology 220: 2136–2148.

    PubMed  Google Scholar 

  • Tseng, M. & M. I. O’Connor, 2016. Predators modify the evolutionary response of prey to temperature change. Biology Letters 11: 20150798.

    Google Scholar 

  • Urabe, J. & N. Waki, 2009. Mitigation of adverse effects of rising CO2 on a planktonic herbivore by mixed algal diets. Global Change Biology 15: 523–531.

    Google Scholar 

  • von Frisch, K., 1938. Zur psychologie des fisch-schwarmes. Die Naturwissenschaften 37: 601–606.

    Google Scholar 

  • Watson, S., S. Lefevre, M. McCormick, P. Domenici, G. Nilsson & P. Munday, 2013. Marine mollusc predator-escape behaviour altered by near-future carbon dioxide levels. Proceedings. Biological Sciences/The Royal Society 281: 20132377.

    Google Scholar 

  • Weber, A. & A. Van Noordwijk, 2002. Swimming behaviour of Daphnia clones: differentiation through predator infochemicals. Journal Of Plankton Research 24: 1335–1348.

    CAS  Google Scholar 

  • Weber, A. K. & R. Pirow, 2009. Physiological responses of Daphnia pulex to acid stress. BMC Physiology 9: 9.

    PubMed  PubMed Central  Google Scholar 

  • Weiss, R. F., 1974. Carbon dioxide in water and seawater: the solubility of a non-ideal gas. Marine Chemistry 2: 203–215.

    CAS  Google Scholar 

  • Weiss, L., S. Kruppert, C. Laforsch & R. Tollrian, 2012. Chaoborus and Gasterosteus anti-predator responses in Daphnia pulex are mediated by independent cholinergic and gabaergic neuronal signals. Plos ONE 7: 1–8.

    Google Scholar 

  • Weiss, L. C., F. Leese, C. Laforsch & R. Tollrian, 2015. Dopamine is a key regulator in the signaling pathway underlying predator-induced defenses in Daphnia’. Proceedings of Biological Sciences/The Royal Society 282: 20151440.

    Google Scholar 

  • Weiss, L. C., L. Pötter, A. Steiger, S. Kruppert, U. Frost & R. Tollrian, 2018. Rising pCO2 in freshwater ecosystems has the potential to negatively affect predator-induced defenses in Daphnia. Current Biology 28: 327–332.

    CAS  PubMed  Google Scholar 

  • Zou, E. & M. Fingerman, 1997. Synthetic estrogenic agents do not interfere with sex differentiation but do inhibit molting of the cladoceran Daphnia magna. Bulletin of Environmental Contamination and Toxicology 58: 596–602.

    CAS  PubMed  Google Scholar 

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Acknowledgements

We thank Paul Abboud for help with experiments, Betsy Bancroft for supplying sticklebacks, and Elizabeth Addis, Betsy Bancroft, Frances Lefcort, and two anonymous reviewers for extremely helpful comments on the manuscript. Funding was provided by the Gonzaga University Science Research Program.

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  1. Biology Department, Gonzaga University, 502 E. Boone Avenue, Spokane, WA, 99258, USA

    Jean-Claude Abboud, Edgar A. Bartolome, Mayra Blanco, Annalise C. Kress, Ian Y. Ellis, Perry K. Yazzolino, Kamrin I. Sorensen, James R. Winslow & Hugh Lefcort

  2. Chemistry Department, Gonzaga University, 502 E. Boone Avenue, Spokane, WA, 99258, USA

    David A. Cleary

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  1. Jean-Claude Abboud
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Abboud, JC., Bartolome, E.A., Blanco, M. et al. Carbon dioxide enrichment alters predator avoidance and sex determination but only sex is mediated by GABAA receptors. Hydrobiologia 829, 307–322 (2019). https://doi.org/10.1007/s10750-018-3841-3

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