Skip to main content
SpringerLink
Log in

Evolutionary history and sex are significant drivers of crayfish demography in resource-limited cave ecosystems

  • Original Paper
  • Published:
Evolutionary Ecology Aims and scope Submit manuscript

Abstract

Obligate and facultative cave species both play significant functional roles in cave ecosystems. Unlike obligate cave species, facultative cave species can persist in habitats both within and outside of caves. However, no comparative demographic model explaining the sustained presence of both obligate and facultative cave species has been provided. We developed a multi-state capture–mark–recapture (CMR) analysis based on 5 years of data collected from caves in northern Alabama, USA to explore differences in survival and reproductive transition probabilities between obligate (Orconectes australis and Cambarus hamulatus) and facultative (C. tenebrosus) cave crayfish. Multi-state CMR analyses revealed that male obligate cave species showed significantly higher rates of transitioning to a reproductive state than male C. tenebrosus, while no differences among species were observed for females. Transitioning into a non-reproductive state, however, was higher for obligate cave species regardless of sex. Apparent survival rates between cave obligates and C. tenebrosus did not differ, suggesting that the larger population sizes of obligate cave species within our study sites may be driven by more successful male reproductive strategies. Our results suggest that obligate cave crayfishes have evolved unique sex-specific reproductive strategies not shared by C. tenebrosus that likely represent a specialized adaptation to the cave environment. Conversely, persistent immigration by surface populations is likely crucial for the sustained presence of facultative species within cave environments.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data availability

The datasets analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Aiken D (1969) Ovarian maturation and egg laying in the crayfish Orconectes virilis: influence of temperature and photoperiod. Can J Zool 47:931–935

    Google Scholar 

  • Ameyaw-Akumfi C (1981) Courtship in the crayfish Procambarus clarkii (Girard) (Decapoda, Astacidea). Crustaceana 40:57–64

    Google Scholar 

  • Aquiloni L, Gherardi F (2008) Extended mother-offspring relationships in crayfish: the return behavior of juvenile Procambarus clarkia. Ethology 114:946–954

    Google Scholar 

  • Boretto J, Cabezas F, Tappari F et al (2014) Reproductive biology of Phymaturus spectabilis (Liolaemidae): females skip reproduction in cold and harsh environments of Patagonia, Argentina. Herpetol Conserv Biol 9:170–180

    Google Scholar 

  • Brewis J, Bowler K (1985) A study of reproductive females of the freshwater crayfish Austropotamobius pallipes. Hydrobiologia 121:145–149

    Google Scholar 

  • Bronikowski A (2000) Experimental evidence for the adaptive evolution of growth rate in the garter snake Thamnophis elegans. Evolution 54:1760–1767

    CAS  PubMed  Google Scholar 

  • Bronikowski A, Arnold S (1999) The evolutionary ecology of life history variation in the garter snake Thamnophis elegans. Ecology 80:2314–2325

    Google Scholar 

  • Burnham K, Anderson D (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York

    Google Scholar 

  • Caswell H (2001) Matrix population models: construction, analysis, and interpretation, 2nd edn. Sinauer Associates Inc, Sunderland

    Google Scholar 

  • Cayuela H, Besnard A, Bonnaire E et al (2014) To breed or not to breed: past reproductive status and environmental cues drive current breeding decisions in a long-lived amphibian. Oecologia 176:107–116

    PubMed  Google Scholar 

  • Chevin L, Hoffmann A (2017) Evolution of phenotypic plasticity in extreme environments. Philos Trans R Soc B: Biol Sci 372:20160138.https://dx.doi.org/10.1098/rstb.2016.0138

    Article  Google Scholar 

  • Choquet R, Lebreton J, Gimenez O et al (2009a) U-CARE: Utilities for performing goodness of fit tests and manipulating capture–recapture data. Ecography 32:1071–1074

    Google Scholar 

  • Choquet R, Rouan L, Pradel R (2009b) Program E-SURGE: a software application for fitting multievent models. In: Thomson DL, Cooch EG, Conroy MJ (eds) Modeling demographic processes in marked populations. Springer, New York, pp 845–865

    Google Scholar 

  • Coulson T, Catchpole E, Albon S et al (2001) Age, sex, density, winter weather, and population crashes in Soay sheep. Science 292:1528–1531

    CAS  PubMed  Google Scholar 

  • Covich A, Thorp J (1991) Crustacea: Introduction and Peracarida. In: Thorp JH, Covich AP (eds) Ecology and classification of North American freshwater invertebrates. Academic Press, San Diego, pp 665–689

    Google Scholar 

  • Culver D (1985) Trophic relationships in aquatic cave environments. Stygologia 1:43–53

    Google Scholar 

  • Engel A (2007) Observations on the biodiversity of sulfidic karst habitats. J Cave Karst Stud 69:187–206

    CAS  Google Scholar 

  • Engen S, Sæther B (2017) r- and K-selection in fluctuating populations is determined by the evolutionary trade-off between two fitness measures: growth rate and lifetime reproductive success. Evolution 71:167–173

    PubMed  Google Scholar 

  • Fagan W, Cosner C, Larsen E et al (2010) Reproductive asynchrony in spatial population models: how mating behavior can modulate Allee effects arising from isolation in both space and time. Am Nat 175:362–373

    PubMed  Google Scholar 

  • Gerber L, White E (2014) Two-sex matrix models in assessing population viability: when do male dynamics matter? J Appl Ecol 51:270–278

    Google Scholar 

  • Gimenez O, Lebreton J, Choquet R et al (2018) R2ucare: An R package to perform goodness-of-fit tests for capture–recapture models. Methods Ecol Evol 9:1749–1754

    Google Scholar 

  • Gutiérrez-Yurrita P, Montes C (1999) Bioenergetics and phenology of reproduction of the introduced red swamp crayfish, Procambarus clarkii, in Doñana National Park, Spain, and implications for species management. Freshw Biol 42:561–574

    Google Scholar 

  • Hayward A, Gillooly J (2011) The cost of sex: Quantifying energetic investment in gamete production by males and females. PLoS ONE 6:e16557

    CAS  PubMed  PubMed Central  Google Scholar 

  • Henderson BA, Trivedi T, Collins N (2000) Annual cycle of energy allocation to growth and reproduction of yellow perch. J Fish Biol 57:122–133

    Google Scholar 

  • Hervant F, Mathieu J, Durand J (2001) Behavioural, physiological and metabolic responses to long-term starvation and refeeding in a blind cave-dwelling (Proteus anguinus) and a surface-dwelling (Euproctus asper) salamander. J Exp Biol 204:269–281

    CAS  PubMed  Google Scholar 

  • Hunter J, Macewicz B, Sibert J (1986) The spawning frequency of skipjack tuna, Katsuwonus pelamis, from the South Pacific. Fish Bull 84:895–903

    Google Scholar 

  • Huntsman B, Venarsky M, Benstead J et al (2011a) Effects of organic matter availability on the life history and production of a top vertebrate predator (Plethodontidae: Gyrinophilus palleucus) in two cave streams. Freshw Biol 56:1746–1760

    Google Scholar 

  • Huntsman B, Venarsky M, Benstead J (2011b) Relating carrion breakdown rates to ambient resource level and community structure in four cave stream ecosystems. J N Am Benthol Soc 30:882–892

    Google Scholar 

  • Hüppop K (2000) How do cave animals cope with the food scarcity in caves? In: Goodall DW, Wilkens H, Culver DC, Humphreys WF (eds) Ecosystems of the world: subterranean ecosystems. Elsevier Science, Amsterdam, pp 159–188

    Google Scholar 

  • Jegla T (1966) Reproductive and molting cycles in cave crayfish. Biol Bull 130:345–358

    Google Scholar 

  • Jenouvrier S, Barbraud C, Cazelles B et al (2005) Modelling population dynamics of seabirds: importance of the effects of climate fluctuations on breeding proportions. Oikos 108:511–522

    Google Scholar 

  • Jurcak A, Lahman S, Wofford S, Moore P (2016) Behavior of crayfish. In: Longshaw M, Stebbing B (eds) Biology and ecology of crayfish. CRC Press, London, pp 117–131

    Google Scholar 

  • Kotliar B, Wiens J (1990) Multiple scales of patchiness and patch structure: a hierarchical framework for the study of heterogeneity. Oikos 59:253–260

    Google Scholar 

  • Lebreton J, Nichols J, Barker R et al (2009) Modeling individual animal histories with multistate capture–recapture models. Adv Ecol Res 41:87–173

    Google Scholar 

  • Leibold M, Holyoak M, Mouquet N et al (2004) The metacommunity concept: a framework for multi-scale community ecology. Ecol Lett 7:601–613

    Google Scholar 

  • Mason J (1970) Copulatory behavior of the crayfish, Pacifastacus trowbridgii (Stimpson). Can J Zool 48:969–976

    Google Scholar 

  • McBride R, Somarakis S, Fitzhugh G et al (2015) Energy acquisition and allocation to egg production in relation to fish reproductive strategies. Fish Fish 16:23–57

    Google Scholar 

  • McLay C, van den Brink A (2016) Crayfish growth and reproduction. In: Longshaw M, Stebbing P (eds) Biology and ecology of crayfish. CRC Press, Boca Raton, pp 62–116

    Google Scholar 

  • Moore M, Riesch R, Martin R (2016) The predictability and magnitude of life-history divergence to ecological agents of selection: a meta-analysis in livebearing fishes. Ecol Lett 19:435–442

    PubMed  Google Scholar 

  • Nichols J, Kendall W (1995) The use of multi-state capture-recapture models to address questions in evolutionary ecology. J Appl Stat 22:835–846

    Google Scholar 

  • Nichols J, Hines J, Lebreton J et al (2000) Estimation of contributions to population growth: a reverse-time capture–recapture approach. Ecology 81:3362–3376

    Google Scholar 

  • O'Brien D, Min T, Larsen T et al (2008) Use of stable isotopes to examine how dietary restriction extends Drosophila lifespan. Curr Biol 18:R155–R156

    CAS  PubMed  Google Scholar 

  • Pianka E (1970) On r- and K-Selection. Am Nat 104:592–597

    Google Scholar 

  • Pippitt M (1977) Mating behavior of the crayfish Orconectes nais (Faxon, 1885) (Decapoda, Astacoidea). Crustaceana 32:265–271

    Google Scholar 

  • Poff N (1997) Landscape filters and species traits: towards mechanistic understanding and prediction in stream ecology. J N Am Benthol Soc 16:391–409

    Google Scholar 

  • Poulson T, White W (1969) The cave environment. Science 165:971–981

    CAS  PubMed  Google Scholar 

  • Prins R (1968) Comparative ecology of the crayfishes Orconectes rusticus and Cambarus tenebrosus in Doe Run, Meade County, Kentucky. Int Rev Hydrobiol 53:667–714

    Google Scholar 

  • R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Rankin D, Kokko H (2007) Do males matter? The role of males in population dynamics. Oikos 116:335–348

    Google Scholar 

  • Rétaux S, Casane D (2013) Evolution of eye development in the darkness of caves: adaptation, drift, or both? EvoDevo 4:26

    PubMed  PubMed Central  Google Scholar 

  • Rideout R, Burton M, Rose G (2000) Observations on mass atresia and skipped spawning in northern Atlantic cod, from Smith Sound, Newfoundland. J Fish Biol 57:1429–1440

    Google Scholar 

  • Robinet C, Lance D, Thorpe K et al (2008) Dispersion in time and space affect mating success and Allee effects in invading gypsy moth populations. J Anim Ecol 77:966–973

    CAS  PubMed  Google Scholar 

  • Rogowski D, Sitko S, Bonar S (2013) Optimizing control of invasive crayfish using life-history information. Freshw Biol 58:1279–1291

    Google Scholar 

  • Sarojini R, Nagabhushanam R, Fingerman M (1995) Naphthalene-induced atresia in the ovary of the crayfish, Procambarus clarkii. Ecotoxicol Environ Saf 31:76–83

    CAS  PubMed  Google Scholar 

  • Schneider K, Christman M, Fagan W (2011) The influence of resource subsidies on cave invertebrates: results from an ecosystem-level manipulation experiment. Ecology 92:765–776

    PubMed  Google Scholar 

  • Simon K, Benfield E (2001) Leaf and wood breakdown in cave streams. J N Am Benthol Soc 20:550–563

    Google Scholar 

  • Simon K, Benfield E, Macko S (2003) Food web structure and the role of epilithic biofilms in cave streams. Ecology 84:2395–2406

    Google Scholar 

  • Soares D, Niemiller M (2013) Sensory adaptations of fishes to subterranean environments. Bioscience 63:274–283

    Google Scholar 

  • Tessier A, Woodruff P (2002) Trading off the ability to exploit rich versus poor food quality. Ecol Lett 5:685–692

    Google Scholar 

  • Tessier A, Leibold M, Tsao J (2000) A fundamental trade-off in resource exploitation by Daphnia and consequences to plankton communities. Ecology 81:826–841

    Google Scholar 

  • Tökölyi J, Bradács F, Hóka N et al (2016) Effects of food availability on asexual reproduction and stress tolerance along the fast–slow life history continuum in freshwater hydra (Cnidaria: Hydrozoa). Hydrobiologia 766:121–133

    Google Scholar 

  • Trippel E, Harvey H (1989) Missing opportunities to reproduce: an energy dependent or fecundity gaining strategy in white sucker (Catostomus commersoni)? Can J Zool 67:2180–2188

    Google Scholar 

  • Venarsky M, Huntsman B (2018) Food webs in caves. In: Moldovan OT, Kovác L, Halse S (eds) Cave ecology. Springer, Cham, pp 309–328

    Google Scholar 

  • Venarsky M, Benstead J, Huryn A (2012a) Effects of organic matter and season on leaf litter colonisation and breakdown in cave streams. Freshw Biol 57:773–786

    Google Scholar 

  • Venarsky M, Huryn A, Benstead J (2012b) Re-examining extreme longevity of the cave crayfish Orconectes australis using new mark–recapture data: a lesson on the limitations of iterative size-at-age models. Freshw Biol 57:1471–1481

    Google Scholar 

  • Venarsky M, Huntsman B, Huryn A et al (2014) Quantitative food web analysis supports the energy-limitation hypothesis in cave stream ecosystems. Oecologia 176:859–869

    PubMed  Google Scholar 

  • Venarsky M, Benstead J, Huryn A et al (2018) Experimental detritus manipulations unite surface and cave stream ecosystems along a common energy gradient. Ecosystems 21:629–642

    CAS  Google Scholar 

  • Veran S, Beissinger S (2009) Demographic origins of skewed operational and adult sex ratios: perturbation analyses of two-sex models. Ecol Lett 12:129–143

    PubMed  Google Scholar 

  • Villanelli F, Gherardi F (1998) Breeding in the crayfish, Austropotamobius pallipes: Mating patterns, mate choice and intermale competition. Freshw Biol 40:305–315

    Google Scholar 

  • Vlaming V (1972) Environmental control of teleost reproductive cycles: a brief review. J Fish Biol 4:131–140

    Google Scholar 

Download references

Acknowledgements

Funding for this project was provided by the University of Alabama and two State Wildlife Grants entitled “Assessment of population dynamics of cave inhabiting crayfish in Alabama” to A.D.H. and B.R.K (Grant # T-03-02 and T-3-3-2). Data for this project were collected under State of Alabama Department of Conservation Permit 2010000029568680. F.A. thanks the New Mexico State Agricultural Experiment Station for financial support (NM Fitsum-2017H). We are grateful to Horace Clemens and the Southeastern Cave Conservancy for cave access. Thanks to Chau Tran, Jim Godwin, Justin Cook, Tom Heatherly, Dr. Michael Kendrick, Randall Blackwood, Stuart W. McGregor, Lauren Showalter, Mica Junior, Dru Holla, Dr. Tim Wynn, Cameron Craig, Samantha Richter, Chase Moon, Jonathan Hopper, Jessica Hopper, James Ramsey, Dr. Mick Demi, Dr. Dan Nelson, Dr. Brook Fluker, Derrick Wells, and Dr. Michael Sandel for their assistance in the field and laboratory. This manuscript was improved by helpful comments by Dr. Michael Sandel. The authors of this manuscript have no conflicts of interest to report.

Author information

Author notes

  1. Brock M. Huntsman

    Present address: California Water Science Center, United States Geological Survey, Sacramento, CA, 95819, USA

  2. Michael P. Venarsky

    Present address: Australian Rivers Institute, Griffith University, Nathan Campus, Nathan, QLD, 4111, Australia

Authors and Affiliations

  1. Department of Biological Sciences, University of Alabama, Tuscaloosa, AL, 35487, USA

    Brock M. Huntsman, Michael P. Venarsky, Alexander D. Huryn & Jonathan P. Benstead

  2. Department of Fish, Wildlife and Conservation Ecology, New Mexico State University, Las Cruces, NM, 88003, USA

    Fitsum Abadi

  3. Tennessee Aquarium Conservation Institute, Chattanooga, TN, 37405, USA

    Bernard R. Kuhajda

  4. Department of Biology, Georgia Southern University, Statesboro, GA, 30458, USA

    Christian L. Cox

Authors
  1. Brock M. Huntsman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michael P. Venarsky
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fitsum Abadi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Alexander D. Huryn
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Bernard R. Kuhajda
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Christian L. Cox
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jonathan P. Benstead
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

BMH, MPV, FA and CLC conceived the ideas; MPV, ADH, BRK, and JPB designed methodology; BMH, MPV, ADH, BRK, and JPB collected data; BMH and FA analyzed the data; BMH led writing of the manuscript; all authors contributed critically to the drafts and gave final approval for publication.

Corresponding author

Correspondence to Brock M. Huntsman.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 368 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Huntsman, B.M., Venarsky, M.P., Abadi, F. et al. Evolutionary history and sex are significant drivers of crayfish demography in resource-limited cave ecosystems. Evol Ecol 34, 235–255 (2020). https://doi.org/10.1007/s10682-019-10029-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-019-10029-w

Keywords

Search

Navigation