Abstract
The Mexican cavefish, Astyanax mexicanus (Characidae), has become an important model in evolutionary physiology and developmental biology, providing insights into the evolution of sensory systems, pigmentation, and metabolism. In contrast, comparatively little is known about the natural history and trophic ecology of this elusive cave inhabitant. We investigated cavefish from three independently colonized cave systems (Pachón, Tinaja, and Sabinos), which are located in the Sierra de El Abra of northeastern Mexico. Samples were collected multiple times throughout the year to investigate variation in body size, sex ratios, proportions of individuals with empty guts, and diet composition. We found consistent differences in body size among caves, and sex ratios were generally female biased, although to varying degrees. Gut content analyses indicated that cavefish consume food throughout the year, and diets are dominated by detritus, plant materials, and aquatic invertebrates. Especially in the Pachón cave, where we had the densest sampling, there was evidence for seasonal changes in diet composition that coincided with the rainy and dry seasons. Our findings potentially suggest that the cave environments in this system are characterized by continual nutrient limitation, rather than intermittent periods of starvation.
Similar content being viewed by others
Data availability
All data associated with this manuscript will be made available in a public repository (Dryad) upon acceptance of the manuscript or can be obtained directly from the corresponding authors.
References
Aspiras AC, Rohner N, Martineau B, Borowsky RL, Tabin CJ (2015) Melanocortin 4 receptor mutations contribute to the adaptation of cavefish to nutrient-poor conditions. Proc Natl Acad Sci U S A 112:9668–9673
Avise JC, Selander RK (1972) Evolutionary genetics of cave-dwelling fishes of the genus Astyanax. Evolution 26:1–19
Bates D, Mächler M, Bolker B, Walker S (2014) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48
Behrmann-Godel J, Nolte AW, Kreiselmaier J, Berka R, Freyhof J (2017) The first European cave fish. Curr Biol 27:R257–R258
Beladjal L, Vandekerckhove TTM, Muyssen B, Heyrman J, de Caesermaeker J, Mertens J (2002) B-chromosomes and male-biased sex ratio with paternal inheritance in the fairy shrimp Branchipus schaefferi (Crustacea, Anostraca). Heredity 88:356–360
Blanckenhorn WU (2000) The evolution of body size: what keeps organisms small? Quart Rev Biol 75:385–407
Borowsky R (2008) Determining the sex of adult Astyanax mexicanus. Cold Spring Harb Protoc 2008:pdb.prot5090
Bradic M, Beerli P, García-de León FJ, Esquivel-Bobadilla S, Borowky RL (2012) Gene flow and population structure in the Mexican blind cavefish complex (Astyanax mexicanus). BMC Evol Biol 12:9
Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York
Christiansen K (2012) Morphological adaptations. In: Culver DC, White WB (eds) Encyclopedia of caves, 2nd ed. Elsevier Academic Press, Amsterdam, pp 517–528
Clark FE, Kocher TD (2019) Changing sex for selfish gain: B chromosomes of Lake Malawi cichlid fish. Sci Rep 9:20213
Cornelio D, Castro JP, Santos MH, Vicari MR, de Almeida MC, Moreira-Filho O, Camacho JP, Artoni RF (2017) Hermaphroditism can compensate for the sex ratio in the Astyanax scabripinnis species complex (Teleostei: Characidae): expanding the B chromosome study model. Rev Fish Biol Fish 27:681–689
Culver DC, Holsinger JR (1969) Preliminary observations on sex ratios in the subterranean amphipod genus Stygonectes (Gammaridae). Am Midl Nat 82:631–633
Culver DC, Kane TC, Fong DW (1995) Adaptation and natural selection in caves. Harvard University Press, Cambridge
Enyidi U, Kiljunen M, Jones RI, Pirhonen J (2013) Nutrient assimilation by first-feeding African catfish, Clarias gariepinus, assessed using stable isotope analysis. J World Aquac Soc 44:161–172
Espinasa L, Borowsky RB (2001) Origins and relationship of cave populations of the blind Mexican tetra, Astyanax fasciatus, in the Sierra de El Abra. Environ Biol Fish 62:233–237
Espinasa L, Bibliowicz J, Jeffery WR, Rétaux S (2014) Enhanced prey capture skills in Astyanax cavefish larvae are independent from eye loss. EvoDevo 5:35
Espinasa L, Bonaroti N, Wong J, Pottin K, Queinnec E, Rétaux S (2017) Contrasting feeding habits of post-larval and adult Astyanax cavefish. Subterr Biol 21:1–17
Espinasa L, Legendre L, Fumey J, Blin M, Rétaux S, Espinasa M (2018) A new cave locality for Astyanax cavefish in Sierra de El Abra, Mexico. Subterr Biol 26:39–53
Espino del Castillo A, Castaño G, Davila-Montes M, Miranda-Anaya M, Morales-Malacara JB, Paredes-León R (2009) Seasonal distribution and circadian activity in the troglophile long-footed robber frog, Eleutherodactylus longipes (Anura: Brachycephalidae) at Los Riscos cave, Querétaro, Mexico: field and laboratory studies. J Cave Karst Stud 71:24–31
Fenolio DB, Graening GO, Collier BA, Stout JF (2006) Coprophagy in a cave-adapted salamander; the importance of bat guano examined through nutritional and stable isotope analyses. Proc R Soc B 273:439–443
Frank SA (1990) Sex allocation theory for birds and mammals. Ann Rev Ecol Syst 21:13–55
Franz-Odendaal TA, Hall BK (2006) Modularity and sense organs in the blind cavefish, Astyanax mexicanus. Evol Dev 8:94–100
Frøland Steindal IA, Beale AD, Yamamoto Y, Whitmore D (2018) Development of the Astyanax mexicanus circadian clock and non-visual light responses. Dev Biol 441:345–354
Fryxell DC, Arnett HA, Apgar TM, Kinnison MT, Palkovacs EP (2015) Sex ratio variation shapes the ecological effects of a globally introduced freshwater fish. Proc R Soc B 282:20151970
Gross JB (2012) The complex origin of Astyanax cavefish. BMC Evol Biol 12:105
Hervant F (2012) Starvation in subterranean species versus surface-dwelling species: crustaceans, fish, and salamanders. In: McCue MD (ed) Comparative Physiology of Fasting, Starvation, and Food Limitation. Springer, Berlin, Heidelberg, pp 91–102
Hervant F, Renault D (2002) Long-term fasting and realimentation in hypogean and epigean isopods: a proposed adaptive strategy for groundwater organisms. J Exp Biol 205:2079–2087
Hinaux H, Devos L, Blin M, Elipot Y, Bibliowicz J, Alié A, Rétaux S (2016) Sensory evolution in blind cavefish is driven by early embryonic events during gastrulation and neurulation. Development 143:4521–4532
Hollister JW (2021) elevatr: access elevation data from various APIs. R package version 0.4.1. https://CRAN.R-project.org/package=elevatr/
Hüppop K (1985) The role of metabolism in the evolution of cave animals. Natl Speleol Soc Bull 47:136–146
Hüppop K (1986) Oxygen consumption of Astyanax fasciatus (Characidae, Pisces): a comparison of epigean and hypogean populations. Environ Biol Fish 17:299–308
Hüppop K (1987) Food-finding ability in cave fish (Astyanax fasciatus). Int J Seleol 16:59–66
Imarazene B, Beille S, Jouanno E, Branthonne A, Thermes V, Thomas M, Herpin A, Rétaux S, Guiguen Y (2020) Primordial germ cell migration and histological and molecular characterization of gonadal differentiation in Pachón cavefish Astyanax mexicanus. Sex Dev 14:80–98
Imarazene B, Du K, Beille S, Jouanno E, Feron R, Pan, Q, Torres-Paz, J, Lopez-Roques C, Castinel A, Gil L, Kuchly C, Donnadieu C, Parrinello H, Journot L, Cabau C, Zahm M, Klopp C, Pavlica T, Al-Rikabi A, Liehr T, Simanovsky SA, Bohlen J, Sember A, Perez J, Veyrunes F, Mueller TD, Postlethwait JH, Schartl M, Herpin A, Rétaux S, Guiguen Y (2021) A supernumerary “B-sex” chromosome drives male sex determination in the Pachón cavefish, Astyanax mexicanus. Curr Biol 31:1–10
Jeffery WR (2009) Regressive evolution in Astyanax cavefish. Ann Rev Genet 43:25–47
Johnson JB, Omland KS (2004) Model selection in ecology and evolution. Trend Ecol Evol 19:101–108
Kasumyan AO, Marusov EA (2015) Chemoorientation in the feeding behavior of the blind Mexican cavefish Astyanax fasciatus (Characidae, Teleostei). Russ J Ecol 46:559–563
Keene A, Yoshizawa M, McGaugh SE (2015) Biology and evolution of the Mexican cavefish. Academic Press, Waltham
Konec M, Prevorčnik S, Sarbu SM, Verovnik R, Trontelj P (2015) Parallels between two geographically and ecologically disparate cave invasions by the same species, Asellus aquaticus (Isopoda, Crustacea). J Evol Biol 28:864–875
Kowalko J (2020) Utilizing the blind cavefish Astyanax mexicanus to understand the genetic basis of behavioral evolution. J Exp Biol 223:jeb208835
Kowalko JE, Rohner N, Linden TA, Rompano SB, Warren WC, Borowsky R, Tabin CJ, Jeffery WR, Yoshizawa M (2013) Convergence in feeding posture occurs through different genetic loci in independently evolved cave populations of Astyanax mexicanus. Proc Natl Acad Sci U S A 110:16933–16938
Lin H-J, Kao W-Y, Wang Y-T (2007) Analyses of stomach contents and stable isotopes reveal food sources of estuarine detritivorous fish in tropical/subtropical Taiwan. Estuar Coast Shelf Sci 73:527–537
McArdle BH, Anderson ML (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82:290–297
Miller RR, Minckley WL, Norris SM (2005) Freshwater fishes of Mexico. University of Chicago Press, Chicago
Mitchell RW, Elliott WR, Russell WH (1977) Mexican eyeless characin fishes, genus Astyanax: environment, distribution, and evolution. Spec Publ Mus Tex Tech 12:1–89
Moore JC, Berlow EL, Coleman DC, de Ruiter PC, Dong Q, Hastings A, Collins Johnson N, McCann KS, Melville KS, Morin PJ, Nadelhoffer K, Rosemond AD, Post DM, Sabo JL, Scow KM, Vanni MJ, Wall DH (2004) Detritus, trophic dynamics and biodiversity. Ecol Lett 7:584–600
Moran D, Softley R, Warrant EJ (2014) Eyeless Mexican cavefish save energy by eliminating the circadian rhythm in metabolism. PLoS One 9:e107877
Natri HM, Merilä J, Shikano T (2019) The evolution of sex determination associated with a chromosomal inversion. Nat Commun 10:145
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2020) vegan: Community ecology package. Version R package version 2.5–7. https://CRAN.R-project.org/package=vegan
Passow CN, Greenway R, Arias-Rodriguez L, Jeyasingh PD, Tobler M (2015) Reduction of energetic demands through modification of body size and routine metabolic rates in extremophile fish. Physiol Biochem Zool 88:371–383
Pérez-Rodríguez R, Esquivel-Bobadilla S, Orozco-Ruíz AM, Olivas-Hernández JL, García-De-León FJ (2021) Genetic structure and historical and contemporary gene flow of Astyanax mexicanus in the Gulf of Mexico slope: a microsatellite-based analysis. PeerJ 9:e10784
Porter ML, Crandall KA (2003) Lost along the way: the significance of evolution in reverse. Trend Ecol Evol 18:541–547
Premate E, Borko Š, Kralj-Fišer S, Jennions M, Fišer Ž, Balázs G, Bíró A, Bračko G, Copilaş‐Ciocianu D, Hrga N, Herczeg G, Rxhepi B, Zagmajster M, Zakšek V, Fromhage L, Fišer C (2021) No room for males in caves: female-biased sex ratio in subterranean amphipods of the genus Niphargus. J Evol Biol 34:1653–1661
R Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Reichard M, Polačik M, Blažek R, Vrtílek M (2014) Female bias in the adult sex ratio of African annual fishes: interspecific differences, seasonal trends and environmental predictors. Evol Ecol 28:1105–1120
Rétaux S, Casane D (2013) Evolution of eye development in the darkness of caves: adaptation, drift, or both? EvoDevo 4:26
Riddle MR, Aspiras AC, Gaudenz K, Peuss R, Sung JY, Martineau B, Peavey M, Box AC, Tabin JA, McGaugh S, Borowsky R, Tabin CJ, Rohner N (2018) Insulin resistance in cavefish as an adaptation to a nutrient-limited environment. Nature 555:647–651
Riddle MR, Boesmans W, Caballero O, Kazwiny Y, Tabin CJ (2018) Morphogenesis and motility of the Astyanax mexicanus gastrointestinal tract. Dev Bio 441:285–296
Roach KA, Tobler M, Winemiller KO (2011) Hydrogen sulfide, bacteria, and fish: a unique, subterranean food chain. Ecology 92:2056–2062
Secor SM (2009) Specific dynamic action: a review of the postprandial metabolic response. J Comp Physiol B 179:1–56
Simon V, Elleboode R, Mahé K, Legendre L, Ornelas-Garcia P, Espinasa L, Rétaux S (2017) Comparing growth in surface and cave morphs of the species Astyanax mexicanus: insights from scales. EvoDevo 8:23
Soares D, Niemiller ML (2013) Sensory adaptations of fishes to subterranean environments. Bioscience 63:274–283
South A (2017) rnaturalearth: world map data from Natural Earth. R package version 0.1.0. https://CRAN.R-project.org/package=rnaturalearth
Tobler M (2008) Divergence in trophic ecology characterizes colonization of extreme habitats. Biol J Linn Soc 95:517–528
Tobler M, Riesch RW, Tobler CM, Plath M (2009) Compensatory behaviour in response to sulphide-induced hypoxia affects time budgets, feeding efficiency, and predation risk. Evol Ecol Res 11:935–948
Tobler M, Scharnweber K, Greenway R, Passow CN, Arias-Rodriguez L, García-De-León (2015) Convergent changes in the trophic ecology of extremophile fish along replicated environmental gradients. Freshw Biol 60:768–780
Trajano E (2001) Ecology of subterranean fishes: an overview. Environ Biol Fish 62:133–160
Whelan CJ, Brown JS (2005) Optimal foraging and gut constraints: reconciling two schools of thought. Oikos 110:481–496
Wilkens H, Burns RJ (1972) A new Anoptichthys cave population (Characidae, Pisces). Ann Spéléol 27:263–270
World Weather Online (2021) Tampico Monthly Climate Averages 2009-present. In: WorldWeatherOnline.com. https://www.worldweatheronline.com/tampico-weather/tamaulipas/mx.aspx. Accessed 30 Aug 2021
Xiong S, Krishnan J, Peuß R, Rohner N (2018) Early adipogenesis contributes to excess fat accumulation in cave populations of Astyanax mexicanus. Dev Biol 441:297–304
Yoshida K, Terai Y, Mizoiri S, Aibara M, Nishihara H, Watanabe M, Kuroiwa A, Hirai H, Hirai Y, Matsuda Y, Okada N (2011) B chromosomes have a functional effect on female sex determination in Lake Victoria cichlid fishes. PLoS Genet 7:e1002203
Yoshizawa M, Gorički Š, Soares D, Jeffery WR (2010) Evolution of a behavioral shift mediated by superficial neuromasts helps cavefish find food in darkness. Curr Biol 20:1631–1636
Acknowledgements
Collection permits provided by the Mexican government (DGOPA.05003.181010-5003; DGOPA.00570.288108-0291; DAPA/2/130409/0961, 230401-613-03). FJGdL thanks the Instituto Tecnológico de Ciudad Victoria and its students who enthusiastically participated in the field collections.
Funding
The field collections were financed by FJGdL. The study was also supported by a grant from the National Science Foundation (IOS-1931657 to MT).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Ethics approval
Our study was conducted at the Technological Institute of Ciudad Victoria (ITCV) in Tamaulipas, México, where despite the lack of any animal care protocol, the animals were all collected under standard care procedures. Authors are responsible for correctness of the statements provided in the manuscript.
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Wilson, E.J., Tobler, M., Riesch, R. et al. Natural history and trophic ecology of three populations of the Mexican cavefish, Astyanax mexicanus. Environ Biol Fish 104, 1461–1474 (2021). https://doi.org/10.1007/s10641-021-01163-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10641-021-01163-y