Modulation of phenotypic traits under different rearing temperatures: Experimental evidence in male guppy (Poecilia reticulata)

Md. Moshiur Rahman, Iva Alam Pinkey, Jannatul Ferthous, Shaikh Tareq Arafat, Sheikh Mustafizur Rahman, Md. Asaduzzaman, Md. Mostafizur Rahman, Muhammad Abdur Rouf

Abstract

Climate change particularly global warming unceasingly imposes a selective pressure in many organisms that results in phenotypic plasticity particularly by expressing different adaptive phenotypes to shifting environmental conditions. The present study was, therefore, conducted to explore the phenotypic responses of male guppy (Poecilia reticulata), a popular model fish, to an ambient (28±0.91°C), high (32±0.12°C) and low (22±0.17°C) rearing temperature. Almost equal sized juvenile males were collected from the wild and reared up to 30 days maintaining necessary conditions similar among treatments except the water temperature. The findings revealed that high-temperature reared fish had significantly lower number of courtships, reduced survival, decreased body size, deformed body shape, limited colour patterns and reduced sperm bundle number than the ambient- and low-temperature groups. On the other hand, low-treatment males performed significantly higher number of courtships than ambient-temperature group, while ambient-temperature reared males possessed significantly higher body size and iridescent colour area than low- temperature treatment. Interestingly, the findings also revealed some trade-offs between traits under thermal-induced stressed conditions (i.e. both high and low temperatures). These findings elicit further information about the thermal condition dependent expression of phenotypic traits of fishes which infer about how fish species will adapt in the predicted changing aquatic environments because of unprecedented climate change.

Keywords

Global warming, Thermal stress, Phenotypic plasticity, Sexual and non-sexual traits, Trade-offs.

Full Text:

PDF

References

Adams D.C., Rohlf F.J., Slice D.E. (2004). Geometric morphometrics: Ten years of progress following the ‘revolution.’ Italian Journal of Zoology, 71(1): 5-16.

Adriaenssens B., van Damme R., Seebacher F., Wilson, R.S. (2012). Sex cells in changing environments: Can organisms adjust the physiological function of gametes to different temperatures? Global Change Biology, 18(6): 1797-1803.

Anacleto P., Figueiredo C., Baptista M., Maulvault A.L., Camacho C., Pousão-Ferreira P., Rosa R. (2018). Fish energy budget under ocean warming and flame retardant exposure. Environmental Research, 164: 186-196.

Angilletta M.J., Wilson R.S. Navas C.A., James, R.S. (2003). Tradeoffs and the evolution of thermal reaction norms. Trends in Ecology and Evolution, 18(5): 234-240.

Araújo M.S., Perez S.I., Magazoni M.J.C., Petry A.C. (2014). Body size and allometric shape variation in the molly Poecilia vivipara along a gradient of salinity and predation. BMC Evolutionary Biology, 14: 1-11.

Armstrong E.J., Tanner R.L., Stillman J.H. (2019). High heat tolerance is negatively correlated with heat tolerance plasticity in nudibranch mollusks. Physiological and Biochemical Zoology, 92(4): 430-444.

Austin J.A., Colman S.M. (2007). Lake Superior summer water temperatures are increasing more rapidly than regional air temperatures: A positive ice-albedo feedback. Geophysical Research Letters, 34(6): L06604.

Bello A.-A.D., Hashim N.B., Haniffah M.R.M. (2017). Predicting impact of climate change on water temperature and dissolved oxygen in tropical rivers. Climate, 5(3): 58.

Bhatt J.P., Kandwal J.S., Nautiyal R. (2002). Water temperature and pH influence olfactory sensitivity to pre-ovulatory and post-ovulatory ovarian pheromones in male Barilius bendelisis. Journal of Biosciences, 27(3): 273-281.

Billerbeck J.M., Schultz E.T., Conover D.O. (2000). Adaptive variation in energy acquisition and allocation among latitudinal populations of the Atlantic silverside. Oecologia, 122(2): 210-219.

Bonte M., Zwolsman J.J.G. (2010). Climate change induced salinisation of artificial lakes in the Netherlands and consequences for drinking water production. Water Research, 44(15): 4411-4424.

Boschetto C., Gasparini C., Pilastro A. (2011). Sperm number and velocity affect sperm competition success in the guppy (Poecilia reticulata). Behavioral Ecology and Sociobiology, 65(4): 813-821.

Breckels R.D., Neff B.D. (2013). The effects of elevated temperature on the sexual traits, immunology and survivorship of a tropical ectotherm. Journal of Experimental Biology, 216(14): 2658-2664.

Brooks R., Endler J.A. (2001). Female guppies agree to differ: phenotypic and genetic variation in mate-choice behavior and the consequences for sexual selection. Evolution, 55(8): 1644-1655.

Buentello J.A., Gatlin D.M., Neill W.H. (2000). Effects of water temperature and dissolved oxygen on daily feed consumption, feed utilization and growth of channel catfish (Ictalurus punctatus). Aquaculture, 182(3-4): 339-352.

Burns J.G., Saravanan A., Helen R.F. (2009). Rearing environment affects the brain size of guppies: lab-reared guppies have smaller brains than wild-caught guppies. Ethology, 115(2): 122-133.

Cattelan S., Pilastro A. (2018). Sperm priming response to perceived mating opportunities is reduced in male guppies with high baseline sperm production. Current Zoology, 64(2): 205-211.

Colchen T., Teletchea F., Fontaine P., Pasquet A. (2016). Temperature modifies activity, inter-individual relationships and group structure in fish. Current Zoology, 63(2): 175-183.

Cole G.L., Endler J.A. (2015). Variable environmental effects on a multicomponent sexually selected trait. The American Naturalist, 185(4): 452-468.

Corral R.W.D., Aguirre W.E. (2019). Effects of temperature and water turbulence on vertebral number and body shape in Astyanax mexicanus (Teleostei: Characidae). PLoS One, 14(7): e0219677.

Cottin D., Roussel D., Foucreau N., Hervant F., Piscart C. (2012). Disentangling the effects of local and regional factors on the thermal tolerance of freshwater crustaceans. Naturwissenschaften, 99(4): 259-264.

Crossin G.T., Hinch S.G., Cooke S.J., Welch D.W., Patterson D.A., Jones S. R.M., … Farrell A.P. (2008). Exposure to high temperature influences the behaviour, physiology, and survival of sockeye salmon during spawning migration. Canadian Journal of Zoology, 86(2): 127-140.

Crozier L.G., Hutchings J.A. (2014). Plastic and evolutionary responses to climate change in fish. Evolutionary Applications, 7(1): 68-87.

Devigili A., Evans J.P., Fitzpatrick J.L. (2019). Predation shapes sperm performance surfaces in guppies. Proceedings of the Royal Society B: Biological Sciences, 286(1905): 20190869.

DeWitt T.J., Sih A., Wilson D.S. (1998). Costs and limits of phenotypic plasticity. Trends in Ecology and Evolution, 13(2): 77-81.

Djurichkovic L.D., Donelson J.M., Fowler A.M., Feary D.A., Booth D.J. (2019). The effects of water temperature on the juvenile performance of two tropical damselfishes expatriating to temperate reefs. Scientific Reports, 9(1): 13937.

Donelson J.M., McCormick M.I., Booth D.J., Munday P.L. (2014). Reproductive acclimation to increased water temperature in a tropical reef fish. PLoS One, 9(5): e97223.

Donelson J.M., Wong M., Booth D.J., Munday P.L. (2016). Transgenerational plasticity of reproduction depends on rate of warming across generations. Evolutionary Applications, 9(9): 1072-1081.

Endler J.A. (1987). Predation, light intensity and courtship behaviour in Poecilia reticulata (Pisces: Poeciliidae). Animal Behaviour, 35(5): 1376-1385.

Endler J.A. (1991). Variation in the appearance of guppy color patterns to guppies and their predators under different visual conditions. Vision Research, 31(3): 587-608.

Evans J.P., Rahman M.M., Gasparini C. (2015). Genotype-by-environment interactions underlie the expression of pre- and post-copulatory sexually selected traits in guppies. Journal of Evolutionary Biology, 28(4): 959-972.

Evans J.P. (2010). Quantitative genetic evidence that males trade attractiveness for ejaculate quality in guppies. Proceedings of the Royal Society B: Biological Sciences, 277(1697): 3195-3201.

Evans J.P., Zane L., Francescato S., Pilastro A. (2003). Directional postcopulatory sexual selection revealed by artificial insemination. Nature, 421(6921): 360-363.

Evans J.P., Magurran A.E. (1999). Geographic variation in sperm production by Trinidadian guppies. Proceedings of the Royal Society of London. Series B: Biological Sciences, 266(1433): 2083-2087.

Evans J.P., Kelley J.L., Bisazza A., Finazzo E., Pilastro A. (2004). Sire attractiveness influences offspring performance in guppies. Proceedings of the Royal Society B: Biological Sciences, 271(1552): 2035-2042.

Farrell A.P., Franklin C.E. (2016). Recognizing thermal plasticity in fish. Science, 351(6269): 132-133.

Fenkes M., Fitzpatrick J.L., Shiels H.A., Nudds R.L. (2019). Acclimation temperature changes spermatozoa flagella length relative to head size in brown trout. Biology Open, 8(7): bio039461.

Flato G.M., Boer G.J. (2001). Warming asymmetry in climate change simulations. Geophysical Research Letters, 28(1): 195-198.

Gamble S., Lindholm A.K., Endler J.A., Brooks R. (2003). Environmental variation and the maintenance of polymorphism: The effect of ambient light spectrum on mating behaviour and sexual selection in guppies. Ecology Letters, 6(5): 463-472.

Gasparini C., Marino I.A.M., Boschetto C., Pilastro A. (2010). Effect of male age on sperm traits and sperm competition success in the guppy (Poecilia reticulata). Journal of Evolutionary Biology, 23(1): 124-135.

Green B.S., Fisher R. (2004). Temperature influences swimming speed, growth and larval duration in coral reef fish larvae. Journal of Experimental Marine Biology and Ecology, 299(1): 115-132.

Grether G.F., Kolluru G.R., Rodd F.H., de la Cerda J., Shimazaki K. (2005). Carotenoid availability affects the development of a colour-based mate preference and the sensory bias to which it is genetically linked. Proceedings of the Royal Society B: Biological Sciences, 272(1577): 2181-2188.

Groot A.T., Zizzari Z.V. (2019). Does climate warming influence sexual chemical signaling? Animal Biology, 69(1): 83-93.

Hemmer-Brepson C., Replumaz L., Romestaing C., Voituron Y., Daufresne M. (2014). Non-stressful temperature effect on oxidative balance and life history traits in adult fish (Oryzias latipes). Journal of Experimental Biology, 217(2): 274-282.

Hendry A.P., Kelly M.L., Kinnison M.T., Reznick D.N. (2006). Parallel evolution of the sexes? Effects of predation and habitat features on the size and shape of wild guppies. Journal of Evolutionary Biology, 19(3): 741-754.

Houde A.E. (1992). Sex-linked heritability of a sexually selected character in a natural population of Poediia reticulata ( Pisces : Poeciliidae ) ( guppies ). Heredity, 69(3): 229-235.

Houde A.E. (1997). Sex, color, and mate choice in guppies. Princeton University Press, Princeton, NJ. 210 p.

Islam M.A., Uddin M.H., Uddin M.J., Shahjahan M. (2019). Temperature changes influenced the growth performance and physiological functions of Thai pangas Pangasianodon hypophthalmus. Aquaculture Reports, 13: 100179.

Ito Y., Momii K. (2015). Impacts of regional warming on long-term hypolimnetic anoxia and dissolved oxygen concentration in a deep lake. Hydrological Processes, 29(9): 2232-2242.

Jin S.-R., Wen B., Chen Z.-Z., Gao J.-Z., Wang L., Liu Y., Liu H.-P. (2019). Sensitivity in the antioxidant system of discus fish (Symphysodon spp.) to cold temperature: Evidence for species-specific cold resistance. BioRxiv, 749705.

Jobling M. (1997). Temperature and growth: Modulation of growth rate via temperature change. In: C.M. Wood, D.G. McDonald (Eds.). Global Warming: Implications for Freshwater and Marine Fish, Cambridge: Cambridge University Press. pp: 225-253.

Johnston I.A., Dunn J. (1987). Temperature acclimation and metabolism in ectotherms with particular reference to teleost fish. Symposia of the Society for Experimental Biology, 41: 67-93.

Karayucel I., Ak O., Karayucel S. (2006). Effect of temperature on sex ratio in guppy Poecilia reticulata (Peters 1860). Aquaculture Research, 37(2): 139-150.

Kaushal S.S., Likens G.E., Jaworski N.A., Pace M.L., Sides A.M., Seekell D., … Wingate R.L. (2010). Rising stream and river temperatures in the United States. Frontiers in Ecology and the Environment, 8(9): 461-466.

Keller-Costa T., Hubbard P.C., Paetz C., Nakamura Y., da Silva J.P., Rato A., … Canario A.V.M. (2014). Identity of a tilapia pheromone released by dominant males that primes females for reproduction. Current Biology, 24(18): 2130-2135.

Kim J.-H., Kim S.K., Hur Y.B. (2019). Temperature-mediated changes in stress responses, acetylcholin-esterase, and immune responses of juvenile olive flounder Paralichthys olivaceus in a bio-floc environment. Aquaculture, 506: 453-458.

Kithsiri H.M.P., Sharma P., Zaidi S.G.S., Pal A.K., Venkateshwarlu G. (2010). Growth and reproductive performance of female guppy, Poecilia reticulata (Peters) fed diets with different nutrient levels. Indian Journal of Fisheries, 57(1): 65-71.

Klingenberg C.P. (2013). Visualizations in geometric morphometrics: How to read and how to make graphs showing shape changes. Hystrix, 24(1): 15-24.

Knott J.F., Sias J.E., Dave E.V., Jacobs J.M. (2019). Seasonal and long-term changes to pavement life caused by rising temperatures from climate change. Transportation Research Record: Journal of the Transportation Research Board, 2673(6): 267-278.

Koch M., Bowes G., Ross C., Zhang X.-H. (2013). Climate change and ocean acidification effects on seagrasses and marine macroalgae. Global Change Biology, 19(1): 103-132.

Kodric-Brown A. (1985). Female preference and sexual selection for male coloration in the guppy (Poecilia reticulata). Behavioral Ecology and Sociobiology, 17: 199-205.

Kodric-Brown A., Nicoletto P. (2001). Female choice in the guppy (Poecilia reticulata): The interaction between male color and display. Behavioral Ecology and Sociobiology, 50(4): 346-351.

Laudien H., Schlieker V. (1981). Temperature dependence of courtship behabiour in the male guppy, Poecilia reticulata. Journal of Thermal Biology, 6(4): 307-314.

Lindén A., Mäntyniemi S. (2011). Using the negative binomial distribution to model overdispersion in ecological count data. Ecology, 92(7): 1414-1421.

Lushchak V.I., Bagnyukova T.V. (2006). Temperature increase results in oxidative stress in goldfish tissues. 2. Antioxidant and associated enzymes. Comparative Biochemistry and Physiology Part C: Toxicology and Pharmacology, 143(1): 36-41.

Manning N.J., Kime D.E. (1985). The effect of temperature on testicular steroid production in the rainbow trout, Salmo gairdneri, in vivo and in vitro. General and Comparative Endocrinology, 57(3): 377-382.

Maoxiao P., Bo Y., Xiaojun L., Donghong N., Tianyi L., Zhiguo D., Jiale L. (2018). Effects of alkalinity and pH on survival, growth, and enzyme activities in juveniles of the razor clam, Sinonovacula constricta. Frontiers in Physiology, 9: 552.

Merilä J., Hendry A.P. (2014). Climate change, adaptation, and phenotypic plasticity: the problem and the evidence. Evolutionary Applications, 7(1): 1-14.

Mogensen S., Post J.R. (2012). Energy allocation strategy modifies growth–survival trade-offs in juvenile fish across ecological and environmental gradients. Oecologia, 168(4): 923-933.

Morrill J.C., Bales R.C., Conklin M.H. (2005). Estimating stream temperature from air temperature: Implications for future water quality. Journal of Environmental Engineering, 131(1): 139-146.

Munoz N.J., Breckels R.D., Neff B.D. (2012). The metabolic, locomotor and sex-dependent effects of elevated temperature on Trinidadian guppies: Limited capacity for acclimation. Journal of Experimental Biology, 215(19): 3436-3441.

Nakano T., Kameda M., Shoji Y., Hayashi S., Yamaguchi T., Sato M. (2014). Effect of severe environmental thermal stress on redox state in salmon. Redox Biology, 2: 772-776.

Nicoletto P.F. (1993). Female sexual response to condition-dependent ornaments in the guppy, Poecilia reticulata. Animal Behaviour, 46(3): 441-450.

Ojaveer E., Kalejs M. (2005). The impact of climate change on the adaptation of marine fish in the Baltic Sea. ICES Journal of Marine Science, 62(7): 1492-1500.

Oufiero C.E., Whitlow K.R. (2016). The evolution of phenotypic plasticity in fish swimming. Current Zoology, 62(5): 475-488.

Pankhurst N.W., King H.R. (2010). Temperature and salmonid reproduction: Implications for aquaculture. Journal of Fish Biology, 76(1): 69-85.

Pepin P. (1991). Effect of temperature and size on development, mortality, and survival rates of the pelagic early life history stages of marine fish. Canadian Journal of Fisheries and Aquatic Sciences, 48(3): 503-518.

Pilastro A., Bisazza A. (1999). Insemination efficiency of two alternative male mating tactics in the guppy Poecilia reticulata. Proceedings of the Royal Society B: Biological Sciences, 266(1431): 1887-1891.

Pörtner H.O., Berdal B., Blust R., Brix O., Colosimo A., De Wachter B., … Zakhartsev M. (2001). Climate induced temperature effects on growth performance, fecundity and recruitment in marine fish: developing a hypothesis for cause and effect relationships in Atlantic cod (Gadus morhua) and common eelpout (Zoarces viviparus). Continental Shelf Research, 21(18-19): 1975-1997.

Pörtner H.O. (2005). Synergistic effects of temperature extremes, hypoxia, and increases in CO2 on marine animals: From Earth history to global change. Journal of Geophysical Research, 110(C9): C09S10.

Pörtner H.O., Bennett A.F., Bozinovic F., Clarke A., Lardies M.A., Lucassen M., … Stillman J.H. (2006). Trade‐offs in thermal adaptation: The need for a molecular to ecological integration. Physiological and Biochemical Zoology, 79(2): 295-313.

Pulgar J.M., Bozinovic F., Ojeda F.P. (2005). Local distribution and thermal ecology of two intertidal fishes. Oecologia, 142(4): 511-520.

R Development Core Team. (2019). R: A language and environment for statistical computing, version 3.6.1. R Foundation for Statistical Computing, Vienna, Austria. Retrived from https://www.r-project.org.

Rahman M.M., Kelley J.L., Evans J.P. (2013). Condition-dependent expression of pre- and postcopulatory sexual traits in guppies. Ecology and Evolution, 3(7): 2197-2213.

Rahman M.M., Turchini G.M., Gasparini C., Norambuena F., Evans J.P. (2014). The expression of pre- and postcopulatory sexually selected traits reflects levels of dietary stress in guppies. PLoS One, 9(8): e105856.

Reeve A.J., Ojanguren A.F., Deacon A.E., Shimadzu H., Ramnarine I.W., Magurran A.E. (2014). Interplay of temperature and light influences wild guppy (Poecilia reticulata) daily reproductive activity. Biological Journal of the Linnean Society, 111(3): 511-520.

Robertson R.M., Money T.G. (2012). Temperature and neuronal circuit function: Compensation, tuning and tolerance. Current Opinion in Neurobiology, 22(4): 724-734.

Roessig J.M., Woodley C.M., Cech J.J., Hansen L.J. (2004). Effects of global climate change on marine and estuarine fishes and fisheries. Reviews in Fish Biology and Fisheries, 14(2): 251-275.

Rome L.C. (1995). Influence of temperature on muscle properties in relation to swimming performance. Journal of Experimental Biology, 154: 73-99.

Rowiński P.K., Mateos-Gonzalez F., Sandblom E., Jutfelt F., Ekström A., Sundström L. F. (2015). Warming alters the body shape of European perch Perca fluviatilis. Journal of Fish Biology, 87(5): 1234-1247.

Rummer J.L., Couturier C.S., Stecyk J.A.W., Gardiner N.M., Kinch J.P., Nilsson G. E., Munday P.L. (2014). Life on the edge: Thermal optima for aerobic scope of equatorial reef fishes are close to current day temperatures. Global Change Biology, 20(4): 1055-1066.

Sandersfeld T., Davison W., Lamare M.D., Knust R., Richter C. (2015). Elevated temperature causes metabolic trade-offs at the whole-organism level in the Antarctic fish Trematomus bernacchii. Journal of Experimental Biology, 218(15): 2373-2381.

Seebacher F., Ducret V., Little A.G., Adriaenssens B. (2015). Generalist–specialist trade-off during thermal acclimation. Royal Society Open Science, 2(1): 140251.

Sfakianakis D.G., Leris I., Laggis A., Kentouri M. (2011). The effect of rearing temperature on body shape and meristic characters in zebrafish (Danio rerio) juveniles. Environmental Biology of Fishes, 92(2): 197-205.

Shah T.K., Saini V.P., Ojha M.L. (2017). Influence of water temperature on phenotypic sex ratio of an ornamental fish Poecilia reticulate. Journal of Entomology and Zoology Studies, 5(3): 1793-1796.

Sheridan J.A., Bickford D. (2011). Shrinking body size as an ecological response to climate change. Nature Climate Change, 1(8): 401-406.

Sogard S.M., Spencer M.L. (2004). Energy allocation in juvenile sablefish: effects of temperature, ration and body size. Journal of Fish Biology, 64(3): 726-738.

Somero G.N. (2010). The physiology of climate change: How potentials for acclimatization and genetic adaptation will determine “winners” and “losers.” Journal of Experimental Biology, 213(6): 912-920.

Stillman J.H. (2003). Acclimation capacity underlies susceptibility to climate change. Science, 301(5629): 65-65.

Taranger G.L., Vikingstad E., Klenke U., Mayer I., Stefansson S.O., Norberg B., Andersson E. (2003). Effects of photoperiod, temperature and GnRHa treatment on the reproductive physiology of Atlantic salmon (Salmo salar L.) broodstock. Fish Physiology and Biochemistry, 28(1-4): 403-406.

Toni M., Angiulli E., Miccoli G., Cioni C., Alleva E., Frabetti F., Maffioli E. (2019). Environmental temperature variation affects brain protein expression and cognitive abilities in adult zebrafish (Danio rerio): A proteomic and behavioural study. Journal of Proteomics, 204: 103396.

Tripathi N., Hoffmann M., Willing E.-M., Lanz C., Weigel D., Dreyer C. (2009). Genetic linkage map of the guppy, Poecilia reticulata, and quantitative trait loci analysis of male size and colour variation. Proceedings of the Royal Society B: Biological Sciences, 276(1665): 2195-2208.

Wenger A.S., Whinney J., Taylor B., Kroon F. (2016). The impact of individual and combined abiotic factors on daily otolith growth in a coral reef fish. Scientific Reports, 6(1): 28875.

West-Eberhard M.J. (2003). Developmental plasticity and evolution. Oxford University Press, New York. 794 p.

Whitehead P.G., Wilby R.L., Battarbee R.W., Kernan M., Wade, A. J. (2009). A review of the potential impacts of climate change on surface water quality. Hydrological Sciences Journal, 54(1): 101-123.

Whitney J.E., Al-Chokhachy R., Bunnell D.B., Caldwell C.A., Cooke S.J., Eliason E.J., Paukert C.P. (2016). Physiological basis of climate change impacts on North American inland fishes. Fisheries, 41(7): 332-345.

Wilson K.L., De Gisi J., Cahill C.L., Barker O.E., Post J.R. (2019). Life‐history variation along environmental and harvest clines of a northern freshwater fish: Plasticity and adaptation. Journal of Animal Ecology, 88(5): 717-733.

Wimberger P.H. (1992). Plasticity of fish body shape. The effects of diet, development, family and age in two species of Geophagus (Pisces: Cichlidae). Biological Journal of the Linnean Society, 45(3): 197-218.

Wood A.H. (1932). The effect of temperature on the growth and respiration of fish embryos (Salmo fario). Journal of Experimental Biology, 9(3): 271-276.

Xiong Y.J., Chen Z.H., Tan S.L. (2013). Relationship between salinity and sea surface temperature in Pearl River Estuary, China. International Geoscience and Remote Sensing Symposium- IGARSS, Melbourne, Australia. pp: 1575-1578.

Yabuki Y., Koide T., Miyasaka N., Wakisaka N., Masuda M., Ohkura M., … Yoshihara Y. (2016). Olfactory receptor for prostaglandin F2α mediates male fish courtship behavior. Nature Neuroscience, 19(7): 897-904.

Yampolsky L.Y., Schaer T.M.M., Ebert D. (2014). Adaptive phenotypic plasticity and local adaptation for temperature tolerance in freshwater zooplankton. Proceedings of the Royal Society B: Biological Sciences, 281(1776): 20132744.

Yu Y., Mainuddin M., Maniruzzaman M., Mandal U.K., Sarangi S.K. (2019). Rainfall and temperature characteristics in the coastal zones of Bangladesh and West Bengal, India. Journal of the Indian Society of Coastal Agricultural Research, 37(2): 12-23.

Yuan X., Zhou Y., Huang Y., Guo W., Johnson D., Jiang Q., Tu Z. (2017). Effects of temperature and fatigue on the metabolism and swimming capacity of juvenile Chinese sturgeon (Acipenser sinensis). Fish Physiology and Biochemistry, 43(5): 1279-1287.

Zahangir M.M., Haque F., Mostakim G.M., Islam M.S. (2015). Secondary stress responses of zebrafish to different pH: Evaluation in a seasonal manner. Aquaculture Reports, 2: 91-96.

Zeebe R.E., Zachos J.C., Caldeira K., Tyrrell T. (2008). Oceans: Carbon emissions and acidification. Science, 321(5885): 51-52.

Refbacks

  • There are currently no refbacks.