Environmental Biology of Fishes

, Volume 100, Issue 3, pp 265–279 | Cite as

Testing metabolic cold adaptation as a driver of warm-water fish species replacement along the river continuum

  • Matthew J. TroiaEmail author
  • Keith B. Gido


Hydrologic and thermal regimes vary along the upstream-to-downstream river continuum and drive the assembly of fish communities. The metabolic cold adaptation (MCA) hypothesis predicts that faster development is adaptive for species exposed to shorter growing seasons. Whether gradients of hydrologic variability and seasonal thermal regime associated with the river continuum operate as environmental filters on species with differing developmental rates remains an untested mechanism of community assembly. We analyzed daily records of stream discharge and modeled stream temperatures to quantify these two gradients of abiotic harshness in Kansas, USA. We then used laboratory experiments to compare temperature-dependent larval development rates among three congeneric cyprinid species that are most abundant in small tributaries (Pimephales promelas), medium tributaries (P. notatus), or river mainstems (P. vigilax). Growing season duration increased with stream size, with temperature exceedance thresholds of 22 and 26 °C lasting 1.4 and 270 times longer, respectively, in eighth order river mainstems compared to second order tributaries. The frequency of small flood pulses within the growing season peaked in mid-order streams, whereas the frequency of large flood pulses within the growing season peaked in low-order streams. Larval development rates increased with incubation temperature, but did not differ predictably among species. These findings, when viewed alongside a companion study, suggest that thermal adaptation and not MCA explains the replacements of Pimephales species along the river continuum. The prominent upstream-to-downstream gradient in growing season duration highlights the need for studies on the evolutionary and ecological significance of this infrequently explored characteristic of the river continuum.


Community turnover Larval development rate Pimephales Species replacements Thermal adaptation Thermal reaction norm 



The authors thank Nate Cathcart, Michael Denk, Sky Hedden, Emily Johnson, Kevin Kirkbride, Josh Perkin, Dustin Shaw, Trevor Starks, Allison Veach, James Whitney, and Rebecca Zheng for field and laboratory assistance. Many private land owners for provided access to streams as well as the Tallgrass Prairie National Preserve, Kansas Department of Wildlife Parks and Tourism, and Joe and Alison Gerken for substantial stream access. The authors thank Jake Schaefer for advice on experimental design and data analysis as well as John Blair and Conservation Fisheries, Inc. for use of equipment and laboratory facilities. This research was funded by the National Science Foundation (DEB#1311183), the Southwestern Association of Naturalists, Prairie Biotic Research Inc., and the Kansas Academy of Science. Brood stocks were collected under the permission of the Kansas Department of Wildlife Parks and Tourism (permit #SC-089-2014) and housed and spawned under the permission of the Kansas State University Institutional Animal Care and Use Committee (permit #2996). This is publication #17-208-J from the Kansas Agricultural Experiment Station. The authors have no conflicts of interest to declare.

Supplementary material

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Table S1 (DOCX 35 kb)
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Fig. S2 (DOCX 376 kb)


  1. Addo‐Bediako A, Chown SL, Gaston KJ (2002) Metabolic cold adaptation in insects: a large‐scale perspective. Funct Ecol 16:332–338. doi: 10.1046/j.1365-2435.2002.00634.x CrossRefGoogle Scholar
  2. Angilletta MJ (2006) Estimating and comparing thermal performance curves. J Therm Biol 31:541–545. doi: 10.1016/j.jtherbio.2006.06.002 CrossRefGoogle Scholar
  3. Angilletta MJ (2009) Thermal adaptation: a theoretical and empirical synthesis. Oxford University Press, OxfordGoogle Scholar
  4. Baumann H, Conover D (2011) Adaptation to climate change: contrasting patterns of thermal-reaction-norm evolution in Pacific versus Atlantic silversides. Proc R Soc B 278:2265–2273. doi: 10.1098/rspb.2010.2479 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Blanck A, Lamouroux N (2007) Large‐scale intraspecific variation in life‐history traits of European freshwater fish. J Biogeogr 34:862–875. doi: 10.1111/j.1365-2699.2006.01654.x CrossRefGoogle Scholar
  6. Braasch ME, Smith PW (1965) Relationships of the topminnows Fundulus notatus and Fundulus olivaceus in the Upper Mississippi River Valley. Copeia 1965:46–53, CrossRefGoogle Scholar
  7. Braaten PJ, Guy CS (2002) Life history attributes of fishes along the latitudinal gradient of the Missouri River. Trans Am Fish Soc 131:931–945. doi: 10.1577/1548-8659(2002)131<0931:LHAOFA>2.0.CO;2 CrossRefGoogle Scholar
  8. Briere JF, Pracros P, Le Roux AY, Pierre JS (1999) A novel rate model of temperature-dependent development for arthropods. Environ Entomol 28:22–29. doi: 10.1093/ee/28.1.22 CrossRefGoogle Scholar
  9. Brown JH, Gillooly JF, Allen AP, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789. doi: 10.1890/03-9000 CrossRefGoogle Scholar
  10. Cade BS (2006) National hydrologic assessment tool (NATHAT). U.S. Geological SurveyGoogle Scholar
  11. Caissie D, El-Jabi N, Satish MG (2001) Modelling of maximum daily water temperatures in a small stream using air temperatures. J Hydrol 251(1):14–28Google Scholar
  12. Carmona-Catot G, Benito J, Garcia-Berthou E (2011) Comparing latitudinal and upstream-downstream gradients: life history traits of invasive mosquitofish. Divers Distrib 17:214–224. doi: 10.1111/j.1472-4642.2011.00743.x CrossRefGoogle Scholar
  13. Chivers DP, Kiesecker JM, Marco A, Devito J, Anderson MT, Blaustein AR (2001) Predator‐induced life history changes in amphibians: egg predation induces hatching. Oikos 92:135–142. doi: 10.1034/j.1600-0706.2001.920116.x CrossRefGoogle Scholar
  14. Clarke A (2003) Costs and consequences of evolutionary temperature adaptation. Trends Ecol Evol 18:573–581. doi: 10.1016/j.tree.2003.08.007 CrossRefGoogle Scholar
  15. Conover DO (1992) Seasonality and the scheduling of life history at different latitudes. J Fish Biol 41:161–178. doi: 10.1111/j.1095-8649.1992.tb03876.x CrossRefGoogle Scholar
  16. Conover DO, Present TMC (1990) Countergradient variation in growth-rate: compensation for length of the growing-season among Atlantic silversides from different latitudes. Oecologia 83:316–324. doi: 10.1007/BF00317554 CrossRefGoogle Scholar
  17. Cross FB, Collins JT (1995) Fishes in Kansas, 2nd edn. University of Kansas, LawrenceGoogle Scholar
  18. Edds DR (1993) Fish assemblage structure and environmental correlates in Nepal’s Gandaki River. Copeia 1993:48–60. doi: 10.2307/1446294 CrossRefGoogle Scholar
  19. Falcone JA, Carlisle DM, Wolock DM, Meador MR (2010) GAGES: a stream gage database for evaluating natural and altered flow conditions in the conterminous United States. Ecology 91:621. doi: 10.1890/09-0889.1 CrossRefGoogle Scholar
  20. Fausch KD, Nakano S, Ishigaki K (1994) Distribution of two congeneric charrs in streams of Hokkaido Island, Japan: considering multiple factors across scales. Oecologia 100:1–12. doi: 10.1007/BF00317124 CrossRefGoogle Scholar
  21. Fischer K, Kölzow N, Höltje H, Karl I (2011) Assay conditions in laboratory experiments: is the use of constant rather than fluctuating temperatures justified when investigating temperature-induced plasticity? Oecologia 166:23–33. doi: 10.1007/s00442-011-1917-0 CrossRefPubMedGoogle Scholar
  22. Fleming IA, Gross MR (1990) Latitudinal clines: a trade-off between egg number and size in Pacific salmon. Ecology 71:2–11. doi: 10.2307/1940241 CrossRefGoogle Scholar
  23. Fullerton AH, Torgersen CE, Lawler JJ, Faux RN, Steel EA, Beechie TJ, Ebersole JL, Leibowitz SG (2015) Rethinking the longitudinal stream temperature paradigm: region‐wide comparison of thermal infrared imagery reveals unexpected complexity of river temperatures. Hydrol Process 29(22):4719–4737Google Scholar
  24. Gardiner NM, Munday PL, Nilsson GE (2010) Counter-gradient variation in respiratory performance of coral reef fishes at elevated temperatures. PLoS One 5:e13299. doi: 10.1371/journal.pone.0013299 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Gillooly JF, Brown JH, West GB, Savage VM, Charnov EL (2001) Effects of size and temperature on metabolic rate. Science 293:2248–2251. doi: 10.1126/science.1061967 CrossRefPubMedGoogle Scholar
  26. Gordon ND, McMahon TA, Finlayson BL, Gippel CJ, Nathan RJ (2004) Stream hydrology: an introduction for ecologists, 2nd edn. John Wiley and Sons Ltd, ChichesterGoogle Scholar
  27. Grossman GD, Ratajczak RE, Farr MD, Wagner CM, Petty JT (2010) Why there are more fish downstream. In: Gido KB, Jackson DA (eds) Community ecology of stream fishes: concepts, approaches, and techniques. American Fisheries Society Symposium 73, Bethesda, p 63–81Google Scholar
  28. Guisan A, Edwards TC, Hastie T (2002) Generalized linear and generalized additive models in studies of species distributions: setting the scene. Ecol Model 157:89–100. doi: 10.1016/S0304-3800(02)00204-1 CrossRefGoogle Scholar
  29. Heming TA (1982) Effects of temperature on utilization of yolk by chinook salmon (Oncorhynchus tshawytscha) eggs and alevins. Can J Fish Aquat Sci 39:184–190. doi: 10.1139/f82-021 CrossRefGoogle Scholar
  30. Hodgkinson I (2005) Terrestrial insects along elevation gradients: species and community responses to altitude. Biol Rev 80:489–513. doi: 10.1017/S1464793105006767 CrossRefGoogle Scholar
  31. Huet M (1959) Profiles and biology of western European streams as related to fish management. Trans Am Fish Soc 88:155–163. doi: 10.1577/1548-8659(1959)88[155:PABOWE]2.0.CO;2 CrossRefGoogle Scholar
  32. Ibañez C, Belliard J, Hughes RM, Irz P, Kamdem‐Toham A, Lamouroux N, Tedesco PA, Oberdorff T (2009) Convergence of temperate and tropical stream fish assemblages. Ecography 32:658–670. doi: 10.1111/j.1600-0587.2008.05591.x CrossRefGoogle Scholar
  33. Kamler E (2002) Ontogeny of yolk-feeding fish: an ecological perspective. Rev Fish Biol Fish 12:79–103. doi: 10.1023/A:1022603204337 CrossRefGoogle Scholar
  34. Kamler E (2005) Parent–egg–progeny relationships in teleost fishes: an energetics perspective. Rev Fish Biol Fish 15:399–421. doi: 10.1007/s11160-006-0002-y CrossRefGoogle Scholar
  35. Maheu A, Poff NL, St‐Hilaire A (2015) A classification of stream water temperature regimes in the conterminous USA. River Res Appl. doi: 10.1002/rra.2906 Google Scholar
  36. Mims MC, Olden JD (2012) Life history theory predicts fish assemblage response to hydrologic regimes. Ecology 93:35–45. doi: 10.1890/11-0370.1 CrossRefPubMedGoogle Scholar
  37. Neuheimer AB, Taggart, CT (2007) The growing degree-day and fish size-at-age: the overlooked metric. Can J Fish Aquat Sci 64(2):375–385. doi: 10.1007/s10641-017-0577-2
  38. Perkin JS, Gido KB, Costigan KH, Daniels MD, Johnson ER (2014) Fragmentation and drying ratchet down Great Plains stream fish diversity. Aquat Conserv 25:639–655. doi: 10.1002/aqc.2501 CrossRefGoogle Scholar
  39. Pflieger WL (1997) The fishes of Missouri. Missouri Department of ConservationGoogle Scholar
  40. Poff NL (1997) Landscape filters and species traits: towards mechanistic understanding and prediction in stream ecology. J N Am Benthol Soc 391–409. doi: 10.2307/1468026
  41. Poff NL, Allan JD (1995) Functional organization of stream fish assemblages in relation to hydrological variability. Ecology 76:606–627. doi: 10.2307/1941217 CrossRefGoogle Scholar
  42. Poff NL, Allan JD, Bain MB, Karr JR, Prestegaard KL, Richter BD, Sparks RE, Stromberg JC (1997) The natural flow regime. Bioscience 47:769–784. doi: 10.2307/1313099 CrossRefGoogle Scholar
  43. Poff NL, Olden JD, Pepin DM, Bledsoe BP (2006) Placing global stream flow variability in geographic and geomorphic contexts. River Res Appl 22:149–166. doi: 10.1002/rra.902 CrossRefGoogle Scholar
  44. R Development Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  45. Rahel FJ, Hubert WA (1991) Fish assemblages and habitat gradients in a Rocky Mountain–Great Plains stream: biotic zonation and additive patterns of community change. Trans Am Fish Soc 120:319–332. doi: 10.1577/1548-8659(1991)120<0319:FAAHGI>2.3.CO;2 CrossRefGoogle Scholar
  46. Richter BD, Baumgartner JV, Powell J, Braun DP (1996) A method for assessing hydrologic alteration within ecosystems. Conserv Biol 10:1163–1174. doi: 10.1046/j.1523-1739.1996.10041163.x CrossRefGoogle Scholar
  47. Schaefer JF, Ryan A (2006) Developmental plasticity in the thermal tolerance of zebrafish Danio rerio. J Fish Biol 69:722–734. doi: 10.1111/j.1095-8649.2006.01145.x CrossRefGoogle Scholar
  48. Schaefer J, Walters A (2010) Metabolic cold adaptation and developmental plasticity in metabolic rates among species in the Fundulus notatus species complex. Funct Ecol 24:1087–1094. doi: 10.1111/j.1365-2435.2010.01726.x CrossRefGoogle Scholar
  49. Schaefer J, Duvernell D, Kreiser B (2011) Shape variability in topminnows (Fundulus notatus species complex) along the river continuum. Biol J Linn Soc 103:612–621. doi: 10.1111/j.1095-8312.2011.01660.x CrossRefGoogle Scholar
  50. Schultz ET, Reynolds KE, Conover DO (1996) Countergradient variation in growth among newly hatched Fundulus heteroclitus: geographic differences revealed by common-environment experiments. Funct Ecol 10:366–374. doi: 10.2307/2390285 CrossRefGoogle Scholar
  51. Taniguchi Y, Nakano S (2000) Condition-specific competition: implications for the altitudinal distribution of stream fishes. Ecology 81:2027–2039. doi: 10.1890/0012-9658(2000)081[2027:CSCIFT]2.0.CO;2 CrossRefGoogle Scholar
  52. Taniguchi Y, Rahel FJ, Novinger DC, Gerow KG (1998) Temperature mediation of competitive interactions among three fish species that replace each other along longitudinal stream gradients. Can J Fish Aquat Sci 55:1894–1901. doi: 10.1139/f98-072 CrossRefGoogle Scholar
  53. Taylor CM, Lienesch PW (1996) Regional parapatry of the congeneric cyprinids Lythrurus snelsoni and L. umbratilus: species replacement along a complex environmental gradient. Copeia 1996:493–497, CrossRefGoogle Scholar
  54. Troia MJ, Gido KB (2014) Towards a mechanistic understanding of fish species niche divergence along a river continuum. Ecosphere 5:1–18. doi: 10.1890/ES13-00399.1 CrossRefGoogle Scholar
  55. Troia MJ, Gido KB (2015) Functional strategies drive community assembly of stream fishes along environmental gradients and across spatial scales. Oecologia 177:545–559. doi: 10.1007/s00442-014-3178-1 CrossRefPubMedGoogle Scholar
  56. Troia MJ, Denk MA, Gido KB (2015a) Temperature-dependent performance as a driver of warmwater fish species replacement along the river continuum. Can J Fish Aquat Sci. doi: 10.1139/cjfas-2015-0094 Google Scholar
  57. Troia MJ, Williams LR, Williams MG, Ford NB (2015b) The process domains concept as a framework for fish and mussel habitat in a coastal plain river of southeastern North America. Ecol Eng 75:484–496. doi: 10.1016/j.ecoleng.2014.12.016 CrossRefGoogle Scholar
  58. Vannote RL, Minshall GW, Cummins KW, Sedell JR, Cushing CE (1980) The river continuum concept. Can J Fish Aquat Sci 37:130–137. doi: 10.1139/f80-017 CrossRefGoogle Scholar
  59. Violle C, Navas ML, Vile D, Kazakou E, Fortunel C, Hummel I, Garnier E (2007) Let the concept of trait be functional! Oikos 116:882–892. doi: 10.1111/j.0030-1299.2007.15559.x CrossRefGoogle Scholar
  60. Vøllestad LA, Lillehammer T (2000) Individual variation in early life-hostory traits in brown trout. Ecol Freshw Fish 9:242–247. doi: 10.1111/j.1600-0633.2000.eff090407.x CrossRefGoogle Scholar
  61. Vonesh JR, Bolker BM (2005) Compensatory larval responses shift trade-offs associated with predator-induced hatching plasticity. Ecology 86:1580–1591. doi: 10.1890/04-0535 CrossRefGoogle Scholar
  62. Wedekind C (2002) Induced hatching to avoid infectious egg disease in whitefish. Curr Biol 12:69–71. doi: 10.1016/S0960-9822(01)00627-3 CrossRefPubMedGoogle Scholar
  63. Winemiller KO, Rose KA (1992) Patterns of life-history diversification in North American fishes: implications for population regulation. Can J Fish Aquat Sci 49:2196–2218. doi: 10.1139/f92-242
  64. Xenopoulos MA, Lodge DM (2006) Going with the flow: using species-discharge relationships to forecast losses in fish biodiversity. Ecology 87:1907–1914. doi: 10.1890/0012-9658(2006)87[1907:GWTFUS]2.0.CO;2 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2017

Authors and Affiliations

  1. 1.Division of BiologyKansas State UniversityManhattanUSA

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