Hostname: page-component-78c5997874-mlc7c Total loading time: 0 Render date: 2024-11-10T16:14:34.139Z Has data issue: false hasContentIssue false

Explaining diversity patterns in dark waters – a study of aquatic caves in Yucatán, Mexico

Published online by Cambridge University Press:  12 July 2019

Barbara Hendus
Affiliation:
Vrije Universiteit Brussel, Department of Biology, Pleinlaan 2, Elsene, 1050, Belgium
Róger Medina-González
Affiliation:
Universidad Autónoma de Yucatán, Facultad de medicina veterinaria y zootecnia, Licenciatura en biología, 4-116 Itzimná, 97100, Mexico
Celia Sélem-Salas
Affiliation:
Universidad Autónoma de Yucatán, Facultad de medicina veterinaria y zootecnia, Licenciatura en biología, 4-116 Itzimná, 97100, Mexico
Bram Vanschoenwinkel*
Affiliation:
Vrije Universiteit Brussel, Department of Biology, Pleinlaan 2, Elsene, 1050, Belgium
*
*Author for correspondence: Bram Vanschoenwinkel, Email: bvanschoenwinkel@gmail.com

Abstract

In the tropics, limestone caves in karstic areas are known for their unique biodiversity. However, many caves remain unstudied and little is known about underlying gradients that determine diversity and biomass in aquatic microhabitats. Here, we sampled zooplankton and benthos in a set of 12 aquatic caves, locally called closed cenotes in Yucatán, Mexico. Our aim was to explain diversity patterns and differences in biomass with particular attention for correlations between bat colony characteristics and other biota. Compared with caves that support photosynthesis, diversity was low with an average of four planktonic and two benthic species in these dark caves. Undetectable phosphorus concentrations in the water suggest this nutrient is limiting. Several associations hint at a potential link between bat abundance and functional guild composition, water quality and aquatic biota. As such, more bats were linked to higher nitrate concentrations. Yet this was not translated to higher invertebrate biomass, probably since phosphorus is limiting. Overall, the trends found in this survey suggest that bats could be important as fertilizers of the caves although mechanistic links that mediate the flux of nutrients need to be confirmed experimentally.

Type
Research Article
Copyright
© Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature cited

Alcocer, J, Lugo, A, Marín, LE and Escobar, E (1998) Hydrochemistry of waters from five cenotes and evaluation of their suitability for drinking-water supplies, northeastern Yucatan, Mexico. Hydrogeology Journal 6, 293301.CrossRefGoogle Scholar
Alonso, M (1996) Crustacea, Branchiopoda. In Ramos, MA, Alba Tercedor, J, Belles I Ros, X, Gosalbez i Noguera, J, Guerra Sierra, A, Macpherson Mayol, E, Martin Piera, F, Serrano Marino, J, and Templado Gonzalez, J (eds), Fauna Iberica Volume 7. Madrid: Museo Nacional de Ciencias Naturales-Consejo Superior de Investigaciones Cientificas, pp. 1486.Google Scholar
Amoros, C (1984) Introduction pratique à la systématique des organismes des eaux continentales françaises – crustacés cladocères. Bulletin Mensuel de la Société Linnéenne de Lyon 53, 71145.Google Scholar
Arita, HT (1996) The conservation of cave-roosting bats in Yucatan, Mexico. Biological Conservation 76, 177185.CrossRefGoogle Scholar
Arita, HT (1997) Species composition and morphological structure of the bat fauna of Yucatan, Mexico. Journal of Animal Ecology 66, 8397.CrossRefGoogle Scholar
Attayde, JL and Bozelli, RL (1998) Assessing the indicator properties of zooplankton assemblages to disturbance gradients by canonical correspondence analysis. Canadian Journal of Fisheries and Aquatic Sciences 55, 17891797.CrossRefGoogle Scholar
Bauer-Gottwein, P, Gondwe, BRN, Charvet, G, Marín, LE, Rebolledo-Vievra, and Merediz-Alonso, G (2011) Review: the Yucatán Peninsula karst aquifer, Mexico. Hydrogeology Journal 19, 507524.CrossRefGoogle Scholar
Baumgӓrtner, D and Rothhaupt, K-O (2003) Predictive length–dry mass regressions for freshwater invertebrates in a pre-alpine lake littoral. International Review of Hydrobiology 88, 453463.CrossRefGoogle Scholar
Boates, JS and Smith, PC (1979) Length-weight relationships, energy content and the efforts of predation on Corophium volutator (Pallas) (Crustacea: Amphipoda). Proceedings of the Nova Scotian Institute of Science 29, 489499.Google Scholar
Botello, A and Alvarez, F (2010) Genetic variation in the stygobitic shrimp Creaseria morleyi (Decapoda: Palaemonidae), evidence of bottlenecks and re-invasions in the Yucatan Peninsula. Biological Journal of the Linnean Society 99, 315325.CrossRefGoogle Scholar
Bowman, TE (1977) A review of the genus Antromysis (Crustacea: Mysidacea), including new species from Jamaica and Oaxaca, México, and a redescription and new records for A. cenotensis. Studies on the caves and cave fauna of the Yucatán Peninsula, Association for Mexican Cave Studies Bulletin 6, 2738.Google Scholar
Bowman, TE and Iliffe, TM (1988) Species of thermosbaenacean crustacean from the Yucatán Peninsula, México. Proceedings of the Biological Society of Washington 101, 221226.Google Scholar
Brucet, S, Boix, D, Quintana, XD, Jensen, E, Nathansen, LW, Trochine, C, Meerhoff, M, Gascón, S and Jeppesen, E (2010) Factors influencing zooplankton size structure at contrasting temperatures in coastal shallow lakes: implications for effects of climate change. Limnology and Oceanography 55, 16971711.CrossRefGoogle Scholar
Brunet, AK and Medellín, RA (2001) The species-area relationship in bat assemblages of tropical caves. Journal of Mammalogy 82, 11141122.2.0.CO;2>CrossRefGoogle Scholar
Camargo-Guerra, T, Escalera-Vázquez, LH and Zambrano, L (2013) Fish community structure dynamics in cenotes of the Biosphere Reserve of Sian Ka’an, Yucatán Peninsula, Mexico. Revista Mexicana de Biodiversidad 84, 901911.CrossRefGoogle Scholar
Carpenter, ES, Gomez, R, Waldien, DL and Sherwin, RE (2014) Photographic estimation of roosting density of Geoffroy’s Rousette fruit bat Rousettus amplexicaudatus (Chiroptera: Pteropodidae) at Monfort Bat Cave, Philippines. Journal of Threatened Taxa 6, 58385844.CrossRefGoogle Scholar
Cervantes-Martinez, A and Gutiérrez-Aguirre, MA (2014) Physicochemistry and zooplankton of two karstic sinkholes in the Yucatan Peninsula, Mexico. Journal of Limnology 74, 382393.Google Scholar
Cervantes-Martinez, A, Elías-Gutiérrez, M and Suárez-Morales, E (2002) Limnological and morphometrical data of eight karstic systems ‘cenotes’ of the Yucatan Peninsula, Mexico, during the dry season (February–May, 2001). Hydrobiologia 482, 167177.CrossRefGoogle Scholar
Courchaine, RJ (1968) Significance of nitrification in stream analysis: effects on the oxygen balance. Journal (Water Pollution Control Federation) 40, 835847.Google Scholar
Culver, DC (1985) Trophic relationships in aquatic cave environments. Stygologia 1, 4353.Google Scholar
Dickson, GW (1975) A preliminary study of heterotrophic microorganisms as factors in substrate selection of troglobitic invertebrates. NSS Bulletin 37, 8993.Google Scholar
Duchamp, JE, Sparks, DW and Swihart, RK (2010) Exploring the “nutrient hot spot” hypothesis at trees used by bats. Journal of Mammalogy 91, 4853.CrossRefGoogle Scholar
Elías-Gutiérrez, M, Suárez-Morales, E, Gutiérrez-Aguirre, MA, Silva-Briano, M, Grandos-Ramírez, JG and Garfias-Espejo, T (2008) Cladocera y Copepoda de las aguas continentales de México: Guia ilustrada . México, D.F.: UNAM, CONABIO, ECOSUR, SEMARNAT-CONACYT, pp. 322.Google Scholar
Emerson, JK and Roark, AM (2007) Composition of guano produced by frugivorous, sanguivorous, and insectivorous bats. Acta Chiropterologica 9, 261267.CrossRefGoogle Scholar
Escobar-Briones, E, Camacho, ME and Alcocer, J (1997) Calliasmata nohochi, new species (Decapoda: Caridea: Hippolytidae), from anchialine cave systems in continental Quintana Roo, México. Journal of Crustacean Biology 17, 733744.CrossRefGoogle Scholar
Ferreira, RL and Martins, RP (1998) Diversity and distribution of spiders associated with bat guano piles in Morrinho Cave (Bahia State, Brazil). Diversity and Distributions 4, 235241.Google Scholar
Fiers, F, Reid, JW, Iliffe, TM and Suárez-Morales, E (1996) New hypogean cyclopoid copepods (Crustacea) from the Yucatán Peninsula, México. Contributions to Zoology 66, 65102.Google Scholar
Gibert, J and Deharveng, L (2002) Subterranean ecosystems: a truncated functional biodiversity. AIBS Bulletin 52, 473481.Google Scholar
Gonzalez, BC, Borda, E, Carvalho, R and Schulze, A (2012) Polychaetes from the Mayan underworld: phylogeny, evolution, and cryptic diversity. Natura Croatica 21, 5153.Google Scholar
Goveas, SW, Miranda, EC, Seena, S and Sridhar, KR (2006) Observations on guano and bolus of Indian flying fox, Pteropus giganteus . Current Science 90, 160162.Google Scholar
Hall, FG (1936) Physical and chemical survey of cenotes of Yucatán. In Pearse, AS, Creaser, AP and Hall, FG (eds), The Cenotes of Yucatán. Washington, DC: Carnegie Institute of Washington, pp. 516.Google Scholar
Halliday, RB (2015) Catalogue of genera and their type species in the mite Suborder Uropodina (Acari: Mesostigmata). Zootaxa 3972, 101147.CrossRefGoogle Scholar
Herrera-Silveira, JA, Comín, FA, López, S and Sánchez, I (1998) Limnological characterization of aquatic ecosystems in Yucatán Peninsula (SE México). Verhandlungen-Internationale Vereinigung für theoretische und angewandte Limnologie 26, 13481351.Google Scholar
James, KR, Cant, B and Ryan, T (2003) Responses of freshwater biota to rising salinity levels and implications for saline water management: a review. Australian Journal of Botany 51, 703713.CrossRefGoogle Scholar
Jimenez, A, Rennie, MD, Sprules, WG and La Rose, J (2011) Temporal changes in the benthic invertebrate community of Lake Simcoe, 1983–2008. Journal of Great Lakes Research 37, 103112.CrossRefGoogle Scholar
Kamp, A and Witte, U (2005) Processing of 13C-labelled phytoplankton in a fine-grained sandy-shelf sediment (North Sea): relative importance of different macrofauna species. Marine Ecology. Progress Series 297, 6170.CrossRefGoogle Scholar
Kasso, M and Balakrishnan, M (2013) Ecological and economic importance of bats (order Chiroptera). ISRN Biodiversity 2013, 19.Google Scholar
MacSwiney, MC, Vilchis, LP, Clarke, FM and Racey, PA (2007) The importance of cenotes in conserving bat assemblages in the Yucatan, Mexico. Biological Conservation 136, 499509.Google Scholar
MacSwiney, MC, Bolívar Cimé, B, Clarke, FM and Racey, PA (2009) Insectivorous bat activity at cenotes in the Yucatan Peninsula, Mexico. Acta Chiropterologica 11, 139147.CrossRefGoogle Scholar
McCauley, E (1984) The estimation of abundance and biomass of zooplankton in samples. In Downing, JA and Rigler, FH (eds), A Manual on Methods for the Assessment of Secondary Productivity in Fresh Waters. 2nd edition. Oxford: Blackwell, pp. 228265.Google Scholar
Mercado-Salas, NF, Morales-Vela, B, Suáarez-Morales, E and Iliffe, TM (2013) Conservation status of the inland aquatic crustaceans in the Yucatan Peninsula, Mexico: shortcomings of a protection strategy. Aquatic Conservation: Marine and Freshwater Ecosystems 23, 939951.CrossRefGoogle Scholar
Méthot, G, Hudon, C, Gagnon, P, Pinel-Alloul, B, Armellin, A and Poirier, A-MT (2012) Macroinvertebrate size–mass relationships: how specific should they be? Freshwater Science 31, 750764.CrossRefGoogle Scholar
Miserendino, ML (2001) Length-mass relationships for macroinvertebrates in freshwater environments of Patagonia (Argentina). Ecología Austral 11, 38.Google Scholar
Nielsen, DL, Brock, MA, Vogel, M and Petrie, R (2008) From fresh to saline: a comparison of zooplankton and plant communities developing under a gradient of salinity with communities developing under constant salinity levels. Marine and Freshwater Research 59, 549559.CrossRefGoogle Scholar
Pace, ML (1986) An empirical analysis of zooplankton community size structure across lake trophic gradients. Limnology and Oceanography 31, 4555.CrossRefGoogle Scholar
Palacios-Vargas, JG and García-Gómez, A (2014) Biodiversidad de Diplura (Hexapoda: Entognatha) en México. Revista Mexicana de Biodiversidad 85, 236242.CrossRefGoogle Scholar
Pescador, ML, Rasmussen, AK and Harris, SC (1995) Identification Manual for the Caddisfly (Trichoptera) Larvae of Florida. Tallahassee, FL: Bureau of Surface Water Management, Florida Department of Environmental Protection.Google Scholar
Perry, E, Marin, L, McClain, J and Velazquez, G (1995) Ring of cenotes (sinkholes), northwest Yucatan, Mexico: its hydrogeologic characteristics and possible association with the Chicxulub impact crater. Geology 23, 1720.2.3.CO;2>CrossRefGoogle Scholar
Petersen, H (1975) Estimation of dry weight, fresh weight, and calorific content of various Collembolan species. Pedobiologia 15, 222243.Google Scholar
Pierson, ED (1998) Tall trees, deep holes, and scarred landscapes: conservation biology of North American bats. In Kunz, TH and Racey, PA (eds), Bat Biology and Conservation. Washington, DC: Smithsonian Institution Press, pp. 309324.Google Scholar
Pohlman, JW, Iliffe, TM and Cifuentes, LA (1997) A stable isotope study of organic cycling and the ecology of an anchialine cave ecosystem. Marine Ecology. Progress Series 155, 1727.CrossRefGoogle Scholar
Pohlman, JW, Cifuentes, LA and Iliffe, TM (2000) Food web dynamics and biogeochemistry of anchialine caves: a stable isotope approach. In Wilkens, H, Culver, D and Humphreys, W (eds), Ecosystems of the World, Volume 30. Subterranean Ecosystems. Amsterdam: Elsevier, pp. 345358.Google Scholar
Sabo, JL, Bastow, JL and Power, ME (2002) Length-mass relationships for adult aquatic and terrestrial invertebrates in a California watershed. Journal of the North American Benthological Society 21, 336343.CrossRefGoogle Scholar
Sample, BE, Cooper, RJ, Greer, RD and Whitmore, RC (1993) Estimation of insect biomass by length and width. American Midland Naturalist 129, 234240.CrossRefGoogle Scholar
Schmitter-Soto, JJ, Comín, FA, Escobar-Briones, E, Herrera-Silveira, J, Alcocer, J, Suárez-Morales, E, Elías-Gutiérrez, M, Díaz-Arce, V, Marín, LE and Steinich, B (2002) Hydrogeochemical and biological characteristics of cenotes in the Yucatan Peninsula (SE Mexico). Hydrobiologia 467, 215228.CrossRefGoogle Scholar
Smirnov, NN and Elías-Gutiérrez, M (2011) Biocenotic characteristics of some Yucatan lentic water bodies based on invertebrate remains in sediments. Inland Water Biology 4, 211217.CrossRefGoogle Scholar
Smith, KGV (1989) An Introduction to the Immature Stages of British Flies. Handbooks for the Identification of British Insects 10 (Part 14). London: Royal Entomological Society of London.Google Scholar
Sridhar, KR, Ashwini, KM, Seena, S and Sreepada, KS (2006) Manure qualities of guano of insectivorous cave bat Hipposideros speoris . Tropical and Subtropical Agroecosystems 6, 103110.Google Scholar
Stief, P (2013) Stimulation of microbial nitrogen cycling in aquatic ecosystems by benthic macrofauna: mechanisms and environmental implications. Biogeosciences 10, 78297846.CrossRefGoogle Scholar
Strauss, EA and Lamberti, GA (2000) Regulation of nitrification in aquatic sediments by organic carbon. Limnology and Oceanography 45, 18541859.CrossRefGoogle Scholar
Strauss, EA, Mitchell, NL and Lamberti, GA (2002) Factors regulating nitrification in aquatic sediments: effects of organic carbon, nitrogen availability, and pH. Canadian Journal of Fisheries and Aquatic Sciences 59, 554563.CrossRefGoogle Scholar
Studier, EH and Wilson, DE (1983) Natural urine concentrations and composition in neotropical bats. Comparative Biochemistry and Physiology Part A: Physiology 75, 509515.CrossRefGoogle Scholar
Thyssen, PJ (2009) Keys for identification of immature insects. In Amendt, J, Goff, ML, Campobasso, CP and Grassberger, M (eds), Current Concepts in Forensic Entomology. Amsterdam: Springer Science, pp. 2542.CrossRefGoogle Scholar
Towers, DJ, Henderson, IM and Veltman, CJ (1994) Predicting dry weight of New Zealand aquatic macroinvertebrates from linear dimensions. New Zealand Journal of Marine and Freshwater Research 28, 159166.CrossRefGoogle Scholar
Van Hengstum, PJ, Reinhardt, EG, Beddows, PA, Schwarcz, HP and Gabriel, JJ (2009) Foraminifera and testate amoebae (thecamoebians) in an anchialine cave: surface distributions from Aktun Ha (Carwash) cave system, Mexico. Limnology and Oceanography 54, 391396.CrossRefGoogle Scholar
Wilson, EM (1980) Physical Geography of the Yucatán Peninsula. Yucatán: A World Apart. Tuscaloosa, AL: University of Alabama Press.Google Scholar
Xu, F-L, Jørgensen, SE and Tao, S (1999) Ecological indicators for assessing freshwater ecosystem health. Ecological Modelling 116, 77106.CrossRefGoogle Scholar
Zalik, NJ and Strong, AM (2008) Effects of hay cropping on invertebrate biomass and the breeding ecology of Savannah Sparrows (Passerculus sandwichensis). The Auk 125, 700710.CrossRefGoogle Scholar
Zambrano, L, Vázquez-Domínguez, E, García-Bedoya, D, Loftus, WF and Trexler, JC (2006) Fish community structure in freshwater karstic water bodies of the Sian Ka’an Reserve in the Yucatán peninsula, México. Ichthyological Exploration of Freshwaters 17, 193206.Google Scholar