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Diversity of edaphic Heteroptera (Hemiptera) over a heterogeneous neotropical landscape

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Abstract

Studies involving Heteroptera biodiversity and ecology are incipient in tropical ecosystems and have mainly focused on taxonomy. We evaluated the relationship between Heteroptera diversity and habitat type, elevation, forest fragment size and periods of the year in the northernmost limit of Neotropical rainforest, Los Tuxtlas. We sampled Heteroptera using pitfall traps installed in pasturelands and forest fragments, which ranged from 25 to 560 ha in size and were located between 150 and 870 m.a.s.l. Heteroptera species richness and abundance were significantly higher in forest fragments than in pasturelands. In addition, Heteroptera species richness and abundance were negatively related to forest fragment size but were not significantly related to elevation. Lastly, species richness and abundance were significantly higher during spring and summer than during autumn and winter. The greater Heteroptera diversity observed in the forest fragments was likely the result of more than half of the species observed being unique to these habitats. This highlights the importance of habitat conservation in the maintenance of Heteroptera diversity. This study expands the incipient ecological knowledge of this group and provides a basis for future Heteroptera research within fragmented landscapes.

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Fig. 1

Reproduced with permission from Adapted from Von Thaden (2014)

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References

  • Altieri MAA, Nichols CI (2004) Biodiversity and pest management in agroecosystems. Haworth Press Inc, New York

    Book  Google Scholar 

  • Andrew NR, Hughes L (2005) Diversity and assemblage structure of phytophagous Hemiptera along a latitudinal gradient: predicting the potential impacts of climate change. Glob Ecol Biogeogr 14:249–262

    Article  Google Scholar 

  • Anu A, Sabu T, Vineesh P (2009) Seasonality of litter insects and relationship with rainfall in a wet evergreen forest in south Western Ghats. J Insect Sci 9:1–10

    Article  Google Scholar 

  • Barcellos A, Schmidt I, Brailovsky H (2008) Abundance and species richness of Coreoidea (Hemiptera: Heteroptera) from Parque Estadual do Turvo, southern Brazil. Neotrop Entomol 37:406–412

    Article  PubMed  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S, Christensen RHB, Singmann H, Dai B, Scheipl F, Grothendieck G, Green P, Fox J (2019) Package ‘lme4’. https://cran.r-project.org/web/packages/lme4/lme4.pdf. Accessed 10 June 2019

  • Benítez-Malvido J, Martínez-Ramos M (2003) Impact of forest fragmentation on understory plant species richness in Amazonia. Conserv Biol 17:389–400

    Article  Google Scholar 

  • Bianchi FM, Mendonça MS Jr, Campos LA (2014) Comparing vegetation types and anthropic disturbance levels in the Atlantic Forest: how do Pentatomoidea (Hemiptera: Heteroptera) assemblages respond? Environ Entomol 43:1507–1513

    Article  CAS  PubMed  Google Scholar 

  • Biedermann R (2002) Leafhoppers (Hemiptera, Auchenorrhyncha) in fragmented habitats. Neue Folge 176:523–530

    Google Scholar 

  • Bowman J, Cappuccino N, Fahrig L (2002) Patch size and population density the effect of immigration behavior. Conserv Ecol 6:1–9

    Google Scholar 

  • Brailovsky H (1990) Revisión del complejo “Althos” (Hemiptera-Heterotera-Coreidae). Publicaciones Especiales del Instituto de Biología 5, Mexico

  • Brailovsky H, Cadena A (1992) Revisión del género Zicca (Hemiptera-Heteroptera-Coreidae-Coreinae-Coreini). Publicaciones Especiales del Instituto de Biología 9, Mexico

  • Brailovsky H, Mayorga C (1994) Hemiptera-Heteroptera de México XLV. La subfamilia Asopinae (Pentatomidae), en la estación de biología tropical “Los Tuxtlas”, Veracruz, México. An Inst Biol Univ Nac Autón Mex, Ser Zool 65:33–43

    Google Scholar 

  • Brailovsky H, Cervantes L, Mayorga C (1992) Hemiptera: Heteroptera de México XLIV. Biología, Estados ninfales y fenología de la tribu Pentatomini (Pentatomidae) en la Estación de Biología Tropical “Los Tuxtlas”, Veracruz. Publicaciones Especiales del Instituto de Biología 9, Mexico

  • Campos LA, Bertolin TBP, Teixeira RA, Martins FS (2009) Diversity of Pentatomoidea (Hemiptera, Heteroptera) in three fragments of Atlantic Forest in southern Santa Catarina, Brazil. Iheringia 99:165–171

    Article  Google Scholar 

  • Cervantes LP (1999) Description of the immature stages, adult morphology and biology of Pantochlora vivida Stal (Heteroptera: Pentatomidae: Edessinae). J N Y Entomol Soc 107:372–385

    Google Scholar 

  • Cervantes LP, Gámez-Virués S (2005) Three species of facultative Myodochini (Lygaeoidea: Rhyparochromidae) associated with figs in Mexico. Proc Entomol Soc Wash 107:362–375

    Google Scholar 

  • Cervantes LP, Gámez-Virués S (2006) Lethaeini (Hemiptera: Lygaeoidea: Rhyparochromidae) associated with figs in Mexico, with the description of a new species of Cistalia. Proc Entomol Soc Wash 108:101–118

    Google Scholar 

  • Chao A, Lin SY (2011) Program CLAM (classification method). Program and user’s guide. http://purl.oclc.org/clam. Accessed 10 June 2019

  • Chazdon RL, Chao A, Colwell RK, Lin SY, Norden N, Letcher SG, Clark DB, Finegan B, Arroyo JP (2011) A novel statistical method for classifying habitat generalists and specialists. Ecology 92:1332–1343

    Article  PubMed  Google Scholar 

  • Chen J, Saunders SC, Crow TR, Naiman RJ, Brosofske KD, Mroz GD, Brookshire BL, Franklin JF (1999) Microclimate in forest ecosystem and landscape ecology—variations in local climate can be used to monitor and compare the effects of different management regimes. Bioscience 49:288–297

    Article  Google Scholar 

  • Clarke KR, Gorley RN (2006) PRIMER v6: user manual/tutorial. PRIMERE, Plymouth

    Google Scholar 

  • Colwell RK (2013) Estimates: Statistical estimation of species richness and shared species from samples. Version 9. http://purl.oclc.org/estimates. Accessed 15 Jan 2019

  • Connor EF, McCoy ED (1979) the statistics and biology of the species-area relationship. Am Nat 113:791–833

    Article  Google Scholar 

  • Coscarón MC, Melo MC, Coddington J, Corronca J (2009) Estimating biodiversity: a case study on true bugs in Argentinian wetlands. Biodivers Conserv 18:1491–1507

    Article  Google Scholar 

  • Davies-Colley RJ, Payne GW, van Elswijk M (2000) Microclimate gradients across a forest edge. N Z J Ecol 24:111–121

    Google Scholar 

  • Dirzo R, Miranda A (1991) El límite boreal de la selva tropical húmeda en el continente americano: contracción de la vegetación y solución de una controversia. Interciencia 16:240–247

    Google Scholar 

  • Drakare S, Lennon JJ, Hillebrand H (2006) The imprint of the geographical, evolutionary and ecological context on species–area relationships. Ecol Lett 9:215–227

    Article  PubMed  Google Scholar 

  • Firmino JVL, Mendonça MDS Jr, Lima IMM, Grazia J (2017) Pentatomidae (Hemiptera: Heteroptera) in herbaceous and shrub strata of Atlantic Forest remnants in Northeastern Brazil. Environ Entomol 46:480–486

    Article  PubMed  Google Scholar 

  • Fleischer SJ, Gaylor MJ, Hue NV (1988) Dispersal of Lygus lineolaris (Heteroptera: Miridae) adults through cotton following nursery host destruction. Environ Entomol 17:533–541

    Article  Google Scholar 

  • Gessé F, Monleon-Getino T, Goula M (2014) Biodiversity analysis of true bug assemblages (Hemiptera, Heteroptera) in four habitats in the Garraf Natural Park (Barcelona, Spain). J Insect Sci 14:1–14

    Article  Google Scholar 

  • Gleason HA (1922) On the relation between species and area. Ecology 3:158–162

    Article  Google Scholar 

  • Gotelli NJ, Cowell RK (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 4:379–391

    Article  Google Scholar 

  • Grazia J, Simões FL, Panizzi AR (2015) Morphology, ontogeny, reproduction, and feeding of true bugs. In: Panizzi AR, Grazia J (eds) True bugs (Heteroptera) of the Neotropics. Springer, New York, pp 21–56

    Chapter  Google Scholar 

  • Guevara-Sada S, Laborde-Dovalí J, Sánchez-Ríos G (2000) La reserva de la Biosfera Los Tuxtlas. UNESCO, Paris

    Google Scholar 

  • Guevara-Sada S, Laborde K, Sánchez G (2004) Los Tuxtlas. El paisaje de la sierra. Instituto de Ecología, Mexico

    Google Scholar 

  • Gutierrez-García G, Ricker M (2011) Climate and climate change in the region of Los Tuxtlas (Veracruz, Mexico): a statistical analysis. Atmósfera 24:347–373

    Google Scholar 

  • Haddad NM, Brudvig LA, Clobert J, Davies KF, Gonzalez A, Holt RD, Lovejoy TE, Sexton JO, Austin MP, Collins CD et al (2015) Habitat fragmentation and its lasting impact on Earth’s ecosystems. Sci Adv 1:1–9

    Article  Google Scholar 

  • Harrel FE (2019) Package “Hmisc”. https://cran.r-project.org/web/packages/Hmisc/Hmisc.pdf. Accessed 20 Jan 2019

  • Henry TJ (2009) Biodiversity of Heteroptera. In: Foottit RG, Adler PH (eds) Insect biodiversity: science and society. Wiley-Blackwell, Chichester, pp 223–263

    Chapter  Google Scholar 

  • Hill MO (1973) Diversity and evenness: a unifying notation and its consequences. Ecology 54:427–431

    Article  Google Scholar 

  • Hill JL, Curran PJ (2003) Area, shape and isolation of tropical forest fragments: effects on tree species diversity and implications for conservation. J Biogeogr 30:1391–1403

    Article  Google Scholar 

  • Hothorn T, Zeileis A, Farebrother RW, Cummins C, Millo G, Mitchell D (2018) Package “lmtest”. https://cran.r-project.org/web/packages/lmtest/lmtest.pdf. Accessed 15 Jan 2019

  • Jost L (2006) Entropy and diversity. Oikos 113:363–375

    Article  Google Scholar 

  • Jurberg J, Galvão C (2006) Biology, ecology and systematics of Triatominae (Heteroptera: Reduviidae) vectors of Chagas disease and implications for human health. Denisia 19:1096–1116

    Google Scholar 

  • Lattin J (1995) The Hemiptera: Heteroptera of the Columbia river basin, western United States. Hawthorne Place Corvallis 503:752–4027

    Google Scholar 

  • Marcon E, Hérault B (2015) Entropart: an R package to measure and partition diversity. J Stat Softw 67:1–26

    Google Scholar 

  • Mayorga-Martínez C (2002) Revisión genérica de la familia Cydnidae (Hemiptera-Heteroptera) en México, con un listado de las especies conocidas. An del Inst Biol Ser Zool 73:157–192

    Google Scholar 

  • Mayorga-Martínez C, Cervantes LP (2006) Cydnidae (Hemiptera: Heteroptera) from the Centro de Investigaciones Costeras La Mancha, Actopan, Veracruz, México. Rev Mex Biodivers 77:205–214

    Google Scholar 

  • Moir ML, Brennan KEC (2007) Using bugs (Hemiptera) as ecological and environmental indicators in forest ecosystems. In: Muñoz SI (ed) Ecology research progress. Nova Science Publishers Inc, New York, pp 79–115

    Google Scholar 

  • Morrone JJ (2015) Halffter’s Mexican transition zone (1962–2014), cenocrons and evolutionary biogeography. J Zool Syst Evol Res 53:249–257

    Article  Google Scholar 

  • Musolin D, Saulich H (1999) Diversity of seasonal adaptations in terrestrial true bugs (Heteroptera) from the temperate zone. Entomol Sci 4:623–639

    Google Scholar 

  • Nichols E, Larsen T, Spector S, Davis AL, Escobar F, Favila M, Vulinec K (2007) Global dung beetle response to tropical forest modification and fragmentation: a quantitative literature review and meta-analysis. Biol Conserv 137:1–19

    Article  Google Scholar 

  • Novotny V, Basset Y (2000) Rare species in communities of tropical insect herbivores: pondering the mystery of singletons. Oikos 89:564–572

    Article  Google Scholar 

  • Olosutean H, Ilie DM (2013) Are semi-aquatic bugs (Heteroptera: Nepomorpha) indicators of hydrological stability of permanent ponds? Aquat Insect 35:105–118

    Article  Google Scholar 

  • Orabi G, Moir ML, Majer JD (2010) Assessing the success of mine restoration using Hemiptera as indicators. Aust J Zool 58:243–249

    Article  Google Scholar 

  • Pal A, Sinha DC, Rastogi N (2012) Gerris spinolae Lethierry and Severin (Hemiptera: Gerridae) and Brachydeutera longipes Hendel (Diptera: Ephydridae): two effective insect bioindicators to monitor pollution in some tropical freshwater ponds under anthropogenic stress. Psyche 2012:818490

    Google Scholar 

  • Panizzi AR, Grazia J (2015) True bugs (Heteroptera) of the neotropics. Springer, Dordrecht

    Book  Google Scholar 

  • Peredo LC (2002) Description, biology, and maternal care of Pachycoris klugii (Heteroptera: Scutelleridae). Fla Entomol 85:464–473

    Article  Google Scholar 

  • R Core Team (2015) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna

  • Saha A, Gupta S (2015) Aquatic and semi-aquatic Hemiptera of three oxbow lakes of Cachar District, Assam, N. E India and their role as bioindicator. J Entomol Zool Stud 3:111–116

    Google Scholar 

  • Sandoval-Ruiz CA, Cervantes-Peredo L, Mendoza-Palmero FS, Ibáñez-Bernal S (2012) The Triatominae (Hemiptera: Heteroptera: Reduviidae) of Veracruz, Mexico: geographic distribution, taxonomic redescriptions and a key. Zootaxa 3487:1–23

    Article  Google Scholar 

  • Schaefer CW, Panizzi AR (2000) Heteroptera of economic importance. CRC Press, Florida

    Book  Google Scholar 

  • Schimdt LS, Barcellos A (2007) Abundance and species richness of Heteroptera (Hemiptera) from Parque Estadual do Turvo, southern Brazil: Pentatomoidea. Iheringia 97:73–79

    Article  Google Scholar 

  • Schowalter TD (2012) Insect responses to major landscape-level disturbance. Annu Rev Entomol 57:1–20

    Article  CAS  PubMed  Google Scholar 

  • Schuh RT, Slater JA (1995) True bugs of the world (Hemiptera: Heteroptera)—classification and natural history. Cornell University Press, New York

    Google Scholar 

  • Siemann E, Tilman D, Haarstad J, Ritchie M (1998) Experimental tests of the dependence of arthropod diversity on plant diversity. Am Nat 152:738–750

    Article  CAS  PubMed  Google Scholar 

  • Silva AP, Fiuza PSF (2000) Fauna de Heteroptera de la “mata do córrego do paraíso”, Viçosa, Minas Gerais, Brasil. II. Patrones temporalis, distribución annual y estacionalidad. An Inst Biol Univ Nac Auton Mex 71:7–19

    Google Scholar 

  • Sobek S, Gobner MM, Scherber C, Steffan-Dewenter I, Tscharntke T (2009) Tree diversity drives abundance and spatiotemporal β-diversity of true bugs (Heteroptera). Ecol Entomol 34:772–782

    Article  Google Scholar 

  • Socha R, Zamek R (2003) Wing morph-related differences in the walking pattern and dispersal in a flightless bug, Pyrrhocoris apterus (Heteroptera). Oikos 100:35–42

    Article  Google Scholar 

  • Summerville KS, Crist TO (2003) Determinants of lepidopteran species diversity and composition in eastern deciduous forests: roles of season, region, and patch size. Oikos 100:134–148

    Article  Google Scholar 

  • Swezey SL, Nieto DJ, Hagler JR, Pickett CH, Bryer JA, Machtley SA (2013) Dispersion, distribution, and movement of Lygus spp. (Hemiptera: Miridae) in trap-cropped organic strawberries. Environ Entomol 42:770–778

    Article  PubMed  Google Scholar 

  • Tscharntke T, Steffan-Dewenter I, Kruess A, Thies C (2002) Characteristics of insect populations on habitat fragments: a mini review. Ecol Res 17:229–239

    Article  Google Scholar 

  • Vasconcellos A, Andreazze R, Almeida AM, Araujo HFP, Oliveira ES, Oliveira U (2010) Seasonality of insects in the semi-arid Caatinga of northeastern Brazil. Rev Bras Entomol 54:471–476

    Article  Google Scholar 

  • Vega-Vela V, Muñoz-Robles CA, Rodríguez-Luna E, López-Acosta JC, Serna-Lagunes R (2018) Analysis of landscape fragmentation in the Los Tuxtlas Biosphere Reserve, Veracruz, Mexico. Ecosistemas y Recur Agropecu 5:227–238

    Article  Google Scholar 

  • Vidal-Acosta V, Ibañez-Bernal S, Martínez-Campos C (2000) Natural Trypanosoma cruzi infection of triatominae bugs associated with human habitations in Mexico. Salud Publica Mex 42:496–503

    Article  CAS  PubMed  Google Scholar 

  • Von Thaden JJV (2014) Análisis de la cobertura de suelo en el área natural protegida de la reserva de la biosfera “Los Tuxtlas”, de los años de 1986 a 2011. Master’s thesis, INECOL, Xalapa

  • Voss SC, Spafford H, Dadour IR (2009) Annual and seasonal patterns of insect succession on decomposing remains at two locations in Western Australia. Forensic Sci Int 193:26–36

    Article  PubMed  Google Scholar 

  • Wolda H (1988) Insect seasonality: why? Ann Rev Ecol Syst 19:261–280

    Article  Google Scholar 

  • Wolda H, O’Brien CW, Stockwell HP (1998) Weevil diversity and seasonally in tropical Panama as deduced from light-trap catches (Coleoptera: Curculionoidea). Smithson Contrib Zool 590:1–79

    Article  Google Scholar 

  • Zurbrugg C, Frank T (2006) Factors influencing bug diversity (Insecta: Heteroptera) in semi-natural habitats. Biodivers Conserv 15:261–280

    Article  Google Scholar 

  • Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York

    Book  Google Scholar 

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Acknowledgements

We thank the UNAM biological station of Los Tuxtlas and R Coates for the logistic support for the achievement of the fieldwork. We thank F Cuevas-Caselín, A Jacome-Hernández, A Díaz and F Armas for help during fieldwork. We thank C Vargas for her help in processing the samples. In addition, we thank F Laborde-Dolaví and JJ Von Thaden, Instituto de Ecología, A.C., for providing the shapes of land cover from the study area, and D Rivera for aiding the map’s confection. We also thank “Consejo Nacional de Ciencia y Tecnología” (CONACYT) for a scholarship to RP Salomão over the course of this study. We would like to thank Editage for English language editing.

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Correspondence to Renato P. Salomão.

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Supplementary material 1 Number of individuals collected for Heteroptera species in each sampling site within Los Tuxtlas, Veracruz, Mexico (XLSX 20 kb)

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Salomão, R.P., Santacruz, J.B. & Favila, M.E. Diversity of edaphic Heteroptera (Hemiptera) over a heterogeneous neotropical landscape. J Insect Conserv 23, 909–920 (2019). https://doi.org/10.1007/s10841-019-00172-8

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