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Using eco-physiological traits to understand the realized niche: the role of desiccation tolerance in Chagas disease vectors

  • Physiological ecology - original research
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Abstract

Small ectotherms, such as insects, with high surface area-to-volume ratios are usually at risk of dehydration in arid environments. We hypothesize that desiccation tolerance in insects could be reflected in their distribution, which is limited by areas with high relative values of water vapor pressure deficit (VPD) (e.g., hot and dry). The main goal of this study was to explore whether incorporation of eco-physiological traits such as desiccation tolerance in arid environments can improve our understanding of species distribution models (SDM). We use a novel eco-physiological approach to understand the distribution and the potential overlap with their fundamental niche in triatomine bugs, Chagas disease vectors. The desiccation dimension for T. infestans, T. delpontei, T. dimidiata, and T. sordida niches seems to extend to very dry areas. For T. vitticeps, xeric areas seem to limit the geographical range of their realized niche. The maximum VPD limits the western and southern distributions of T. vitticeps, T. delpontei, and T. patagonica. All species showed high tolerance to desiccation with survival times (35 °C-RH ~ 15%) ranging from 24 to 38 days, except for T. dimidiata (9 days), which can be explained by a higher water-loss rate, due to a higher cuticular permeability along with a higher critical water content. This approach indicates that most of these triatomine bugs could be exploiting the dryness dimension of their fundamental niche. Incorporating such species-specific traits in studies of distribution, range, and limits under scenarios of changing climate could enhance predictions of movement of disease-causing vectors into novel regions.

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References

  • Araújo M, Ferri-Yáñez F, Bozinovic F, Marquet P, Valladares F, Chown S (2013) Heat freezes niche evolution. Ecol Lett 16:1206–1219

    Article  PubMed  Google Scholar 

  • Balsalobre A (2016) Ph-D Thesis: ¿Qué especies de vinchucas modificarán su distribución geográfica en la Argentina? Un análisis de los microhábitats y microclimas de los triatominos vectores de la enfermedad de Chagas. Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata, Argentina

  • Belliard S (2015) Degree Thesis. Plasticidad de la tolerancia térmica por aclimatación en la vinchuca Rhodnius prolixus. Universidad de Buenos Aires, Argentina

  • Benoit J, Denlinger D (2010) Meeting the challenges of on-host and off-host water balance in blood-feeding arthropods. J Insect Physiol 56(10):1366–1376

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buckley L, Urban M, Angilletta M, Crozier L, Rissler L, Sears M (2010) Can mechanism inform species’ distribution models? Ecol Lett 13(8):1041–1054

    PubMed  Google Scholar 

  • Bujan J, Yanoviak SP, Kaspari M (2016) Desiccation resistance in tropical insects: causes and mechanisms underlying variability in a Panama ant community. Ecol Evol 6(17):6282–6291

    Article  PubMed  PubMed Central  Google Scholar 

  • Bulleri F, Bruno JF, Silliman BR, Stachowicz JJ (2016) Facilitation and the niche: implications for coexistence, range shifts and ecosystem functioning. Funct Ecol 30(1):70–78

    Article  Google Scholar 

  • Carcavallo RU, Curto de Casas SI, Sherlock IA, Galíndez-Girón I, Jurberg J, Galvão C, Noireau F (1999) Geographical distribution and alti-latitudinal dispersion. Atlas Chagas Dis Vect Am 3:747–792

    Google Scholar 

  • Chown S, Nicolson S (2004) Insect physiological ecology. Oxford University Press, New York, p 244

    Book  Google Scholar 

  • Chown S, Sørensen J, Terblanche J (2011) Water loss in insects: an environmental change perspective. J Insect Physiol 57(8):1070–1084

    Article  CAS  PubMed  Google Scholar 

  • Clark N (1935) The effect of temperature and humidity upon the eggs of the bug, Rhodnius prolixus (Heteroptera, Reduviidae). J Anim Ecol 4:82–87

    Article  Google Scholar 

  • Coast GM (2009) Neuroendocrine control of ionic homeostasis in blood-sucking insects. J Exp Biol 212:378–386

    Article  CAS  PubMed  Google Scholar 

  • Colwell RK, Rangel TF (2009) Hutchinson’s duality: the once and future niche. Proc Natl Acad Sci USA 106(Suppl. 2):19651–19658

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de la Vega GJ, Schilman PE (2017) Ecological and physiological thermal niches in vectors of Chagas disease. Med Vet Entomol. doi:10.1111/mve.12262

    Google Scholar 

  • de la Vega GJ, Medone P, Ceccarelli S, Rabinovich J, Schilman PE (2015) Geographical distribution, climatic variability and thermo-tolerance of Chagas disease vectors. Ecography 38(8):851–860

    Article  Google Scholar 

  • de Souza R, Diotaiuti L, Lorenzo M, Gorla DE (2010) Analysis of the geographical distribution of Triatoma vitticeps (Stal, 1859) based on data of species occurrence in Minas Gerais, Brazil. J Infec Genet Evol 10(6):720–760

    Article  Google Scholar 

  • Denny M (2016) Ecological mechanics. Principles of life’s physical interactions. Princeton University Press, Princeton

    Google Scholar 

  • Diniz-Filho JAF, Ceccarelli S, Hasperué W, Rabinovich J (2013) Geographical patterns of Triatominae (Heteroptera: Reduviidae) richness and distribution in the Western Hemisphere. Insect Conserv Divers 6:704–714

    Article  Google Scholar 

  • Edney E (1977) Water balance in land arthropods. Springer, Germany

    Book  Google Scholar 

  • Elith J, Kearney M, Phillips S (2010) The art of modelling range-shifting species. Methods Ecol Evol 1(4):330–342

    Article  Google Scholar 

  • Felsenstein J (1985) Phylogenies and comparative method. Am Nat 125(1):1–15

    Article  Google Scholar 

  • Fergnani P, Ruggiero A, Ceccarelli S, Menu F, Rabinovich J (2013) Large-scale patterns in morphological diversity and species assemblages in Neotropical Triatominae (Heteroptera: Reduviidae). Mem Inst Oswaldo Cruz 108(8):997–1008

    Article  PubMed  PubMed Central  Google Scholar 

  • Fourcade Y, Engler JO, Rödder D, Secondi J (2014) Mapping species distributions with MAXENT using a geographically biased sample of presence data: a performance assessment of methods for correcting sampling bias. PLoS One 9(5):e97122

    Article  PubMed  PubMed Central  Google Scholar 

  • Gibbs A (2002) Water balance in desert Drosophila: lessons from non-charismatic. Comp Biochem Physiol Part A 133:781–789

    Article  Google Scholar 

  • Gouveia S, Hortal J, Tejedo M, Duarte H, Cassemiro F, Navas C, Diniz-filho JAF (2014) Climatic niche at physiological and macroecological scales: the thermal tolerance geographical range interface and niche dimensionality. Glob Ecol Biogeogr 23:446–456

    Article  Google Scholar 

  • Graham CH, Hijmans RJ (2006) A comparison of methods for mapping species ranges and species richness. Glob Ecol Biogeogr 15(6):578–587

    Article  Google Scholar 

  • Gurgel-Gonçalves R, Galvao C, Costa J, Peterson AT (2012) Geographic distribution of Chagas disease vectors in Brazil based on ecological niche modeling. J Trop Med 2012:1–15

    Article  Google Scholar 

  • Hadley NF (1994) Water relations of terrestrial arthropods. Academic Press Inc, San Diego, California, p 356

    Google Scholar 

  • Hijmans RJ, van Etten J (2015) raster: Geographic data analysis and modeling. R package version 2(1-49):2013

    Google Scholar 

  • Hijmans RJ, Phillips S, Leathwick J, Elith J (2015) dismo: Species distribution modeling. R package version 1.0-12

  • Hill M, Hoffmann A, Macfadyen S, Umina P, Elith J (2012) Understanding niche shifts: using current and historical data to model the invasive redlegged earth mite, Halotydeus destructor. ‎Divers Distrib 18(2):191–203

    Article  Google Scholar 

  • Hutchinson GE (1957) Concluding remarks. Cold Spring Harb Symp Quant Biol 22:415–427

    Article  Google Scholar 

  • Hypsa V, Tietz D, Zrzavý J, Rego R, Galvao C, Jurberg J (2002) Phylogeny and biogeography of Triatominae (Hemiptera: Reduviidae): molecular evidence of a New World origin of the Asiatic clade. Mol Phylogenet Evol 23(3):447–457

    Article  CAS  PubMed  Google Scholar 

  • Intergovernmental Panel on Climate Change (2014) Impacts, adaptation and vulnerability: regional aspects. Cambridge University Press, New York

    Google Scholar 

  • Jiménez-Valverde A, Lobo JM (2007) Threshold criteria for conversion of probability of species presence to either-or presence-absence. Acta Oecol 31:361–369

    Article  Google Scholar 

  • Jurenka R, Terblanche JS, Klok CJ, Chown SL, Krafsur ES (2007) Cuticular lipid mass and desiccation rates in Glossina pallidipes: interpopulation variation. Physiol Entomol 32(3):287–293

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kearney M (2006) Habitat, environment and niche: what are we modelling? Oikos 115(1):186–191

    Article  Google Scholar 

  • Kleynhans E, Terblanche J (2009) The evolution of water balance in Glossina (Diptera: Glossinidae): correlations with climate. Biol Lett 5:93–96

    Article  PubMed  Google Scholar 

  • Kleynhans E, Terblanche J (2011) Complex interactions between temperature and relative humidity on water balance of adult tsetse (Glossinidae, Diptera): implications for climate change. Front Physiol 2(74):1–10

    Google Scholar 

  • Klok J, Chown S (1997) Critical Thermal Limits, Temperature Tolerance and Water Balance of a Sub-Antarctic Caterpillar, Pringleophaga marioni (Lepidoptera: Tineidae). J Insect Physiol 43(7):685–694

    Article  CAS  Google Scholar 

  • Lapinski W, Tschapka M (2014) Desiccation resistance reflects patterns of microhabitat choice in a Central American assemblage of wandering spiders. J Exp Biol 217(15):2789–2795

    Article  PubMed  Google Scholar 

  • Lorenzo M, Lazzari CR (1999) Temperature and relative humidity affect the selection of shelters by Triatoma infestans, vector of Chagas disease. Acta Trop 72:241–249

    Article  CAS  PubMed  Google Scholar 

  • Losos JB (2008) Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. Ecol Lett 11(10):995–1003

    Article  PubMed  Google Scholar 

  • Luz C, Fargues J, Grunewald J (1999) Development of Rhodnius prolixus (Hemiptera: Reduviidae) under constant and cyclic conditions of temperature and humidity. Mem Inst Oswaldo Cruz 94(3):403–409

    Article  CAS  PubMed  Google Scholar 

  • Lyons CL, Coetzee M, Terblanche J, Chown S (2012) Thermal limits of wild and laboratory strains of two African malaria vector species, Anopheles arabiensis and Anopheles funestus. Malar J 11:226

    Article  PubMed  PubMed Central  Google Scholar 

  • Mac Arthur R (1984) Geographical ecology: patterns in the distribution of species. Harper and Row, New York, p 288

    Google Scholar 

  • Martin P, Lefebvre M (1995) Malaria and climate: sensitivity of potential transmission to climate. Ambio 24(4):200–207

    Google Scholar 

  • Mitchell T, Carter T, Jones P, Hulme M, New M (2004) A comprehensive set of climate scenarios for Europe and the globe: the observed record (1900–2000) and 16 scenarios (2000–2100). University of East Anglia, Norwich, p 30

    Google Scholar 

  • Monahan WB (2009) A mechanistic niche model for measuring species’ distributional responses to seasonal temperature gradients. PLoS One 4(11):e7921

    Article  PubMed  PubMed Central  Google Scholar 

  • Nenzén HK, Araújo MB (2011) Choice of threshold alters projections of species range shifts under climate change. Ecol Modell 222(18):3346–3354

    Article  Google Scholar 

  • Orme D (2013) The caper package: comparative analysis of phylogenetics and evolution in R. R package version 5(2):1–36

    Google Scholar 

  • Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Modell 190(3):231–259

    Article  Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D (2014) The nlme package: linear and nonlinear mixed effects models. R package version 3:1–131

  • Pires H, Lazzari CR, Schilman PE, Diotaiuti L, Lorenzo M (2002) Dynamics of thermopreference in the Chagas disease vector Panstrongylus megistus (Hemiptera: Reduviidae). J Med Entomol 39(5):716–719

    Article  CAS  PubMed  Google Scholar 

  • R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Richmond O, McEntee J, Hijmans R, Brashares J (2010) Is the climate right for pleistocene rewilding? Using species distribution models to extrapolate climatic suitability for mammals across continents. PLoS One 5(9):e12899

    Article  PubMed  PubMed Central  Google Scholar 

  • Roca M, Lazzari CR (1994) Effects of the relative humidity on the haematophagous bug Triatoma infestans. Higropreference and eclosion success. J Insect Physiol 40:901–907

    Article  Google Scholar 

  • Rolandi C, Schilman PE (2012) Linking global warning, metabolic rate of haematophagous vectors and the transmission of infectious diseases. Front Physiol 3(75):1–3

    Google Scholar 

  • Rolandi C, Iglesias M, Schilman PE (2014) Metabolism and water loss rate of the haematophagous insect Rhodnius prolixus: effect of starvation and temperature. ‎J. Exp Biol 217:4414–4422

    Article  Google Scholar 

  • Schilman PE, Lighton JRB, Holway DA (2005) Respiratory and cuticular water loss in insects with continuous respiration: comparison across five different ant species. J Insect Physiol 51(12):1295–1305

    Article  CAS  PubMed  Google Scholar 

  • Schilman PE, Lighton JRB, Holway D (2007) Water balance in the Argentine ant (Linepithema humile) compared with five common native ant species from southern California. Physiol Entomol 32(1):1–7

    Article  Google Scholar 

  • Schilman PE, Minoli S, Lazzari CR (2009) The adaptive value of hatching towards the end of the night: lessons from eggs of the haematophagous bug Rhodnius prolixus. Physiol Entomol 34(3):231–237

    Article  Google Scholar 

  • Svenning J, Normand S, Kageyama M (2008) Glacial refugia of temperate trees in Europe: insights from species distribution modelling. J Ecol 96(6):1117–1127

    Article  Google Scholar 

  • Tee H, Lee C (2015) Water balance profiles, humidity preference and survival of two sympatric cockroach egg parasitoids Evania appendigaster and prostocetus hagenowii (Hymenoptera: Evaniidae; Eulophidae). J Insect Physiol 77:45–54

    Article  CAS  PubMed  Google Scholar 

  • Tingley R, Vallinoto M, Sequeira F, Kearney M (2014) Realized niche shift during a global biological invasion. Proc Natl Acad Sci USA 111(28):10233–10238

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weldon CW, Boardman L, Marlin D, Terblanche JS (2016) Physiological mechanisms of dehydration tolerance contribute to the invasion potential of Ceratitis capitata (Wiedemann) (Diptera: Tephritidae) relative to its less widely distributed congeners. Front Zool 13:15

    Article  PubMed  PubMed Central  Google Scholar 

  • WHO Expert Committee World Health Organization (2002) Control of Chagas disease Second report of the WHO. Tech Rep Ser 905:1–119

    Google Scholar 

  • Wigglesworth VB (1945) Transpiration through the cuticle of insects. J Exp Biol 21(3–4):97–114

    Google Scholar 

  • Zachariassen K (1996) The water conserving physiological compromise of desert insects. Eur J Entomol 3:359–367

    Google Scholar 

  • Zuur A, Ieno E, Elphick C (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1(1):3–14

    Article  Google Scholar 

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Acknowledgements

The authors thanks to Dr. Brian Aukema and Jake Wittman from the Aukema Lab (http://www.forest-insects.umn.edu) for critical reading of the manuscript, Amir Dyzenchauz for English corrections, Carmen Rolandi for helping with figures, and Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT, Argentina) (PICT2008-0035 and PICT2008-0268) and CONICET for past financial support. We also thank two anonymous reviewers and a handling editor, whose constructive comments improved the paper.

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Conceived the idea and designed the experiments: PES and GJdlV. Experimental assay: GJdlV and PES. Data analysis: GJdlV. Led the writing of the manuscript: GJdlV. Contributed reagents/materials: PES.

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Correspondence to Pablo E. Schilman.

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All applicable institutional and/or national guidelines for the care and use of animals were followed.

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Communicated by Sylvain Pincebourde.

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de la Vega, G.J., Schilman, P.E. Using eco-physiological traits to understand the realized niche: the role of desiccation tolerance in Chagas disease vectors. Oecologia 185, 607–618 (2017). https://doi.org/10.1007/s00442-017-3986-1

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