Identification of trophic niches of subterranean diving beetles in a calcrete aquifer by DNA and stable isotope analyses
Tessa M. Bradford A B , William F. Humphreys B D E , Andrew D. Austin B and Steven J. B. Cooper B C F
+ Author Affiliations
- Author Affiliations
A CSIRO Land and Water, Urrbrae, SA 5064, Australia.
B Australian Centre for Evolutionary Biology and Biodiversity, and School of Earth and Environmental Sciences, The University of Adelaide, Adelaide, SA 5005, Australia.
C Evolutionary Biology Unit, South Australian Museum, North Terrace, Adelaide, SA 5000, Australia.
D Collections and Research Centre, Western Australian Museum, Welshpool, WA 6106, Australia.
E School of Animal Biology, University of Western Australia, Nedlands, WA 6907, Australia.
F Corresponding author. Email: Steve.Cooper@samuseum.sa.gov.au
Marine and Freshwater Research 65(2) 95-104 https://doi.org/10.1071/MF12356
Submitted: 18 December 2012 Accepted: 1 July 2013 Published: 8 August 2013
Abstract
The Yilgarn calcrete aquifers in Western Australia are an interesting system for investigating the process of speciation within subterranean habitats, because of the limited opportunities for dispersal between isolated calcretes. The presence of different-sized diving beetles (Dytiscidae) in separate calcretes, including sympatric sister-species pairs, suggests that species may have evolved within calcretes by an adaptive shift as a result of ecological-niche differentiation. We have studied the potential for trophic niche partitioning in a sister triplet of diving beetles, of distinctly different sizes, from a single aquifer. Fragments of the mitochondrial COI gene, specific to known species of amphipods and copepods, were polymerase chain reaction-amplified from each of the three beetle species, indicating that there is an overlap in their prey items. Significant differences were found in the detected diets of the three species, and results showed a propensity for prey preferences of amphipods by the large beetles and one species of copepod for the small beetles. A terrestrial source of carbon to the calcrete was suggested by stable isotope analyses. The combined approach of molecular, stable isotope and behavioural studies have provided insight into the trophic ecology of this difficult-to-access environment, providing a framework for more fine-scale analyses of the diet of different-sized species to examine speciation underground.
Additional keywords: amphipods, Chiltoniidae, copepods, dietary analysis, Harpacticoida, stable isotopes, stygofauna, Yilgarn calcrete aquifers.
References
Alarie, Y., Michat, M. C., and Watts, C. H. (2009). Larval morphology of Paroster Sharp, 1882 (Coleoptera: Dytiscidae: Hydroporinae): reinforcement of the hypothesis of monophyletic origin and discussion of phenotypic accommodation to a hypogaeic environment. Zootaxa 2274, 1–44.Allford, A., Cooper, S. J. B., Humphreys, W. F., and Austin, A. D. (2008). Diversity and distribution of groundwater fauna in a calcrete aquifer: does sampling method influence the story? Invertebrate Systematics 22, 127–138.
| Diversity and distribution of groundwater fauna in a calcrete aquifer: does sampling method influence the story?Crossref | GoogleScholarGoogle Scholar |
Anderson, M. J., Gorley, R. N., and Clarke, K. R. (2008). ‘PERMANOVA+ for PRIMER: Guide to Software and Statistical Methods.’ (PRIMER-E: Plymouth, UK.)
Balke, M., Watts, C. H. S., Cooper, S. J. B., Humphreys, W. F., and Vogler, A. P. (2004). A highly modified stygobiont diving beetle of the genus Copelatus (Coleoptera, Dytiscidae): taxonomy and cladistic analysis based on mitochondrial DNA sequences. Systematic Entomology 29, 59–67.
| A highly modified stygobiont diving beetle of the genus Copelatus (Coleoptera, Dytiscidae): taxonomy and cladistic analysis based on mitochondrial DNA sequences.Crossref | GoogleScholarGoogle Scholar |
Bohlke, J. K., and Coplen, T. B. (1995). Interlaboratory comparison of reference materials for nitrogen-isotope-ratio measurements. In ‘Reference and Intercomparison Materials for Stable Isotopes of Light Elements, International Atomic Energy Agency, IAEA TECDOC-825’. pp. 51–66. (Isotope Hydrology Section, IAEA: Vienna.)
Bradford, T., Adams, M., Humphreys, W. F., Austin, A. D., and Cooper, S. J. B. (2010). DNA barcoding of stygofauna uncovers cryptic amphipod diversity in a calcrete aquifer in Western Australia’a arid zone. Molecular Ecology Resources 10, 41–50.
| DNA barcoding of stygofauna uncovers cryptic amphipod diversity in a calcrete aquifer in Western Australia’a arid zone.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1ans7k%3D&md5=86274239de1f75ef8db65985ef440b84CAS | 21564989PubMed |
Bradford, T. M., Adams, M., Guzik, M. T., Humphreys, W. F., Austin, A. D., and Cooper, S. J. B. (2013). Patterns of population genetic variation in sympatric chiltoniid amphipods within a calcrete aquifer reveal a dynamic subterranean environment. Heredity 111, 77–85.
| 1:CAS:528:DC%2BC3sXpsVyrsb0%3D&md5=40d05d387ef8e745f3e1ea462f10b681CAS | 23549336PubMed |
Bray, J. R., and Curtis, J. T. (1957). An ordination of the upland forest communities of southern Wisconsin. Ecological Monographs 27, 325–349.
| An ordination of the upland forest communities of southern Wisconsin.Crossref | GoogleScholarGoogle Scholar |
Burns, A., and Walker, K. F. (2000). Biofilms as food for decapods (Atyidae, Paleomonidae) in the River Murray, South Australia. Hydrobiologia 437, 83–90.
| Biofilms as food for decapods (Atyidae, Paleomonidae) in the River Murray, South Australia.Crossref | GoogleScholarGoogle Scholar |
Castro, A., and Delgado, J. A. (2001). Iberoporus cermenius, a new genus and species of subterranean water beetle (Coleoptera: Dytiscidae) from Spain. Aquatic Insects 23, 33–43.
| Iberoporus cermenius, a new genus and species of subterranean water beetle (Coleoptera: Dytiscidae) from Spain.Crossref | GoogleScholarGoogle Scholar |
Christiansen, K. (2004). Adaptation: morphological (external). In ‘Encyclopedia of Caves and Karst Science’. (Ed. J. Gunn.) pp. 7–9. (Taylor & Francis: Boca Raton, FL, USA.)
Clarke, K. R., and Gorley, R. N. (2006). ‘Primer v6: User Manual/Tutorial.’ (PRIMER-E: Plymouth, UK.)
Clarke, K. R., and Green, R. H. (1988). Statistical design and analysis for a biological effects study. Marine Ecology Progress Series 46, 213–226.
| Statistical design and analysis for a biological effects study.Crossref | GoogleScholarGoogle Scholar |
Cooper, S. J. B., Hinze, S., Leys, R., Watts, C. H. S., and Humphreys, W. F. (2002). Islands under the desert: molecular systematics and evolutionary origins of stygobitic water beetles (Coleoptera: Dytiscidae) from central Western Australia. Invertebrate Systematics 16, 589–598.
| Islands under the desert: molecular systematics and evolutionary origins of stygobitic water beetles (Coleoptera: Dytiscidae) from central Western Australia.Crossref | GoogleScholarGoogle Scholar |
Coplen, T. B. (1995). Reporting of stable hydrogen, carbon, and oxygen isotopic abundances – (technical report). Geothermics 24, 707–712.
| Reporting of stable hydrogen, carbon, and oxygen isotopic abundances – (technical report).Crossref | GoogleScholarGoogle Scholar |
Coplen, T. B., Brand, W. A., Gehre, M., Groning, M., Meijer, H. A. J., Toman, B., and Verkouteren, R. M. (2006). New guidelines for δ13C measurements. Analytical Chemistry 78, 2439–2441.
| New guidelines for δ13C measurements.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhsVSqs7c%3D&md5=eff266273fab08ef4446b50a47571217CAS | 16579631PubMed |
Culver, D. C., and Pipan, T. (2009). ‘The Biology of Caves and Other Subterranean Habitats.’ (Oxford University Press: Oxford, UK.)
Culver, D. C., Kane, T., and Fong, D. W. (1995) ‘Adaptation and Natural Selection in Caves: the Evolution of Gammarus minus.’ (Harvard University: Cambridge, MA.)
Ehleringer, J. R., Rundel, P. W., and Nagy, K. A. (1986). Stable isotopes in physiological ecology and food web research. Trends in Ecology & Evolution 1, 42–45.
| Stable isotopes in physiological ecology and food web research.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7gvFGjsg%3D%3D&md5=603e10cdade68d9e66985ccaa8ebfe4aCAS |
Fenwick, G. D., Thorpe, H. R., and White, P. A. (2004). Groundwater systems. In ‘Freshwaters of New Zealand’. Chapter 29.1–29.18. (Eds J. Harding, P. Mosely, C. Pearson and B. Sorrell.) (New Zealand Hydrological Society and New Zealand Limnological Society: Christchurch, New Zealand.
Fisher, R. A. (1954). ‘Statistical Methods for Research Workers.’ (Oliver and Boyd: Edinburgh, UK.)
Folmer, O., Black, M., Hoeh, W., Lutz, R., and Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 194–199.
Guzik, M. T., Cooper, S. J. B., Humphreys, W. F., and Austin, A. D. (2009). Fine-scale comparative phylogeography of a sympatric sister species triplet of subterranean diving beetles from a single calcrete aquifer in Western Australia. Molecular Ecology 18, 3683–3698.
| Fine-scale comparative phylogeography of a sympatric sister species triplet of subterranean diving beetles from a single calcrete aquifer in Western Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1WhtrbM&md5=cfcd5fa750877ab7bb6fb81b8a9e2b04CAS | 19674311PubMed |
Guzik, M. T., Cooper, S. J. B., Humphreys, W. F., Ong, S., Kawakami, T., and Austin, A. D. (2011). Evidence for population fragmentation within a subterranean aquatic habitat in the Western Australian desert. Heredity 107, 215–230.
| Evidence for population fragmentation within a subterranean aquatic habitat in the Western Australian desert.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MjmslSjtQ%3D%3D&md5=a32588b7a8bc15c87edb0cb920f353d2CAS | 21343944PubMed |
Hancock, P. J., Randall, J. H., and Boulton, A. J. (2009). Preface: hydrogeoecology, the interdisciplinary study of groundwater dependent ecosystems. Hydrogeology Journal 17, 1–3.
| Preface: hydrogeoecology, the interdisciplinary study of groundwater dependent ecosystems.Crossref | GoogleScholarGoogle Scholar |
Hasegawa, M., Kishino, H., and Yano, T. (1985). Dating of human–ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution 22, 160–174.
| Dating of human–ape splitting by a molecular clock of mitochondrial DNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXmtFSns7g%3D&md5=6c91a86b729555395c8c113e18421109CAS | 3934395PubMed |
Humphreys, W. F. (1999). Pysio-chemical profile and energy fixation in Bundera sinkhole, an anchialine remiped habitat in north-western Australia. Journal of the Royal Society of Western Australia 82, 89–98.
Humphreys, W. F. (2001). The subterranean fauna of Barrow Island, northwestern Australia, and its environment. International Journal of Subterranean Biology 28, 107–127.
Humphreys, W. F., Watts, C. H., Cooper, S. J. B., and Leijs, R. (2009). Groundwater estuaries of salt lakes: buried pools of endemic biodiversity on the western plateau, Australia. Hydrobiologia 626, 79–95.
| Groundwater estuaries of salt lakes: buried pools of endemic biodiversity on the western plateau, Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjt1alur8%3D&md5=999f542fe4135bcdf31d51200f762c27CAS |
Jarman, S. N. (2004). AMPLICON: software for designing PCR primers on aligned DNA sequences. Bioinformatics 20, 1644–1645.
| AMPLICON: software for designing PCR primers on aligned DNA sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltlOqtLg%3D&md5=3afc0766f1e0ebbf603f48ecfc16d7f1CAS | 14962918PubMed |
Juan, C., Guzik, M. T., Jaume, D., and Cooper, S. J. B. (2010). Evolution in caves: Darwin’s ‘wrecks of ancient life’ in the molecular era. Molecular Ecology 19, 3865–3880.
| Evolution in caves: Darwin’s ‘wrecks of ancient life’ in the molecular era.Crossref | GoogleScholarGoogle Scholar | 20637049PubMed |
Juen, A., and Traugott, M. (2005). Detecting predation and scavenging by DNA gut-content analysis: a case study using a soil insect predator–prey system. Oecologia 142, 344–352.
| Detecting predation and scavenging by DNA gut-content analysis: a case study using a soil insect predator–prey system.Crossref | GoogleScholarGoogle Scholar | 15517409PubMed |
Kendall, C. (1998). Tracing nitrogen sources and cycles in catchments. In ‘Isotope Tracers in Catchment Hydrology’. (Eds C. Kendall and J. J. McDonnell.) pp. 519–576. (Elsevier: Amsterdam.)
King, R. A., Read, D. S., Traugott, M., and Symondson, W. O. C. (2008). Molecular analysis of predation: a review of best practice for DNA-based approaches. Molecular Ecology 17, 947–963.
| Molecular analysis of predation: a review of best practice for DNA-based approaches.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXktVajurw%3D&md5=bb40c7ff6a1d2272740be9acc53b5a73CAS | 18208490PubMed |
King, R. K., Bradford, T., Austin, A., Humphreys, W. F., and Cooper, S. J. B. (2012). Divergent molecular lineages and not-so-cryptic species: the first descriptions of stygobitic chiltoniid amphipods (Talitroidea: Chiltoniidae) from Western Australia. Journal of Crustacean Biology 32, 465–488.
| Divergent molecular lineages and not-so-cryptic species: the first descriptions of stygobitic chiltoniid amphipods (Talitroidea: Chiltoniidae) from Western Australia.Crossref | GoogleScholarGoogle Scholar |
Larson, D. J., Alarie, Y., and Roughley, R. E. (2000). ‘Predaceous Diving Beetles (Coleoptera: Dytiscidae) of the Nearctic Region, with Emphasis on the Fauna of Canada and Alaska.’ (NRC Research Press: Ottawa, Ontario, Canada.)
Leijs, R., van Nes, E. H., Watts, C. H., Cooper, S. J. B., Humphreys, W. F., and Hogendoorn, K. (2012). Evolution of blind beetles in isolated aquifers: a test of alternative modes of speciation. PLoS ONE 7, e34260.
| Evolution of blind beetles in isolated aquifers: a test of alternative modes of speciation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xlslehtbg%3D&md5=0a9c6041cb16e2f3a9ab08b5f6031ea3CAS | 22479581PubMed |
Leys, R., and Watts, C. H. (2008). Systematics and evolution of the Australian subterranean hydroporine diving beetles (Dytiscidae), with notes on Carabhydrus. Invertebrate Systematics 22, 217–225.
| Systematics and evolution of the Australian subterranean hydroporine diving beetles (Dytiscidae), with notes on Carabhydrus.Crossref | GoogleScholarGoogle Scholar |
Leys, R., Watts, C. H., Cooper, S. J., and Humphreys, W. F. (2003). Evolution of subterranean diving beetles (Coleoptera: Dytiscidae: Hydroporini, Bidessini) in the arid zone of Australia. Evolution 57, 2819–2834.
| 14761060PubMed |
Malard, F., Plénet, S., and Gibert, J. (1996). The use of invertebrates in ground water monitoring: a rising research field. Ground Water Monitoring and Remediation 16, 103–113.
| The use of invertebrates in ground water monitoring: a rising research field.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xjslers7w%3D&md5=b49a3c4692f6073f54ffe34c56de218dCAS |
Pohlman, J. W. (1997). A stable isotope study of organic cycling and the ecology of an anchialine cave ecosystem. Marine Ecology Progress Series 155, 17–27.
| A stable isotope study of organic cycling and the ecology of an anchialine cave ecosystem.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmt12hsLY%3D&md5=d49d9cbdc48dbb9b5c270c4df9f1f71dCAS |
Pompanon, F., Deagle, B. E., Symondson, W. O. C., Brown, D. S., Jarman, S. N., and Taberlet, P. (2012). Who is eating what: diet assessment using next generation sequencing. Molecular Ecology 21, 1931–1950.
| Who is eating what: diet assessment using next generation sequencing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XptVGktr4%3D&md5=fa66058ae403db2c66d2a346850ce2beCAS | 22171763PubMed |
Rundle, H. D., and Nosil, P. (2005). Ecological speciation. Ecology Letters 8, 336–352.
Schluter, D. (2001). Ecology and the origin of species. Trends in Ecology & Evolution 16, 372–380.
| Ecology and the origin of species.Crossref | GoogleScholarGoogle Scholar |
Schluter, D. (2009). Evidence for ecological speciation and its alternative. Science 323, 737–741.
| Evidence for ecological speciation and its alternative.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlert78%3D&md5=cf92f86d3d96528fc14501e3ddbd2218CAS | 19197053PubMed |
Schoener, T. W. (1974). Resource partitioning in ecological communities. Science 185, 27–39.
| Resource partitioning in ecological communities.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cvgslehtQ%3D%3D&md5=1b7b31e1eca6abf41407df972629dfbfCAS | 17779277PubMed |
Sheppard, S. K., and Harwood, J. D. (2005). Advances in molecular ecology: tracking trophic links through predator–prey food-webs. Functional Ecology 19, 751–762.
| Advances in molecular ecology: tracking trophic links through predator–prey food-webs.Crossref | GoogleScholarGoogle Scholar |
Simon, K. S., Benfield, E. F., and Macko, S. A. (2003). Food web structure and the role of epilithic biofilms in cave streams. Ecology 84, 2395–2406.
| Food web structure and the role of epilithic biofilms in cave streams.Crossref | GoogleScholarGoogle Scholar |
Swofford, D. L. (2002). ‘PAUP* Phylogenetic Analysis Using Parsimony (*and Other Methods).’ Version 4.0b10. (Sinauer Associates: Sunderland, MA.)
Symondson, W. O. C. (2002). Molecular identification of prey in predator diets. Molecular Ecology 11, 627–641.
| Molecular identification of prey in predator diets.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XktFaiu7k%3D&md5=e5e2b0558028415a1e0394964fe54727CAS |
Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F., and Higgins, D. G. (1997). The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876–4882.
| The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXntFyntQ%3D%3D&md5=9e6d447216ab1876a878582189669f49CAS | 9396791PubMed |
U’eno, S.-I. (1957). Blind aquatic beetles of Japan, with some accounts of the fauna of Japanese subterranean waters. Archiv fuer Hydrobiologie 53, 250–296.
Vergnon, R., Leijs, R., van Nes, E., and Scheffer, M. (2013). Repeated parallel evolution reveals limiting similarity in subterranean diving beetles. American Naturalist 182, 67–75.
| 23778227PubMed |
Watts, C. H. S., and Humphreys, W. F. (2004). Thirteen new Dytiscidae (Coleoptera) of the genera Boongurrus Larson, Tjirtudessus Watts and Humphreys and Nirripirti Watts and Humphreys, from underground waters in Australia. Transactions of the Royal Society of South Australia 128, 99–129.
Watts, C. H. S., and Humphreys, W. F. (2006). Twenty-six new Dytiscidae (Coleoptera) of the genera Limbodessus Guignot and Nirripirti Watts and Humphreys, from underground waters in Australia. Transactions of the Royal Society of South Australia 130, 123–185.
Watts, C. H. S., and Humphreys, W. F. (2009). Fourteen new Dytiscidae (Coleoptera) of the genera Limbodessus Guignot, Paroster Sharp, and Exocelina Broun from underground waters in Australia. Transactions of the Royal Society of South Australia 133, 62–107.
Wellborn, G. A., and Cothran, R. D. (2007). Niche diversity in crustacean cryptic species: complementarity in spatial distribution and predation risk. Oecologia 154, 175–183.
| Niche diversity in crustacean cryptic species: complementarity in spatial distribution and predation risk.Crossref | GoogleScholarGoogle Scholar | 17684770PubMed |
West, J. B., Bowen, G. J., Cerling, T. E., and Ehleringer, J. R. (2006). Stable isotopes as one of nature’s ecological recorders. Trends in Ecology & Evolution 21, 408–414.
| Stable isotopes as one of nature’s ecological recorders.Crossref | GoogleScholarGoogle Scholar |
