Revista de Biología Tropical ISSN Impreso: 0034-7744 ISSN electrónico: 2215-2075

Invertebrates as disturbance bioindicators in the Manu Biosphere Reserve
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Amaru-Castelo, J., Echevarria-Macassi, L. A., Marquina-Montesinos, E., Herrera-Huayhua, C.-M., & Bautista-Challco, B. (2024). Invertebrates as disturbance bioindicators in the Manu Biosphere Reserve. Revista De Biología Tropical, 72(1), e56199.


Introduction: Monitoring bioindicators is crucial for conservation in natural protected areas, such as the Manu Biosphere Reserve. Different taxa have been used as bioindicators due to their specific characteristics, including ease of sampling, varied responses to disturbances, association richness with other species, and accessible taxonomy. Objectives: To compare the potential of four taxa (Chilopoda, Scarabeidae, Carabidae, and Pompilidae) as bioindicators in a disturbance gradient, considering their ease of collection, presence of changes in community composition, species with marked disturbance preferences, and diversity correlated with other groups. Methods: The study was conducted at the Manu Learning Centre Biological Station within the Manu Biosphere Reserve, a self-regeneration forest with varying degrees of disturbance. Specimens were collected using pitfall traps, yellow pan traps, Malaise traps, and monoliths. Specific richness, abundance, similarity analysis, non-metric multidimensional scaling, Bray-Curtis distance, Bray-Curtis beta diversity partitioning, correspondence analysis, Williams' G goodness-of-fit, and Spearman's correlation index were measured. Results: Among all taxa, the most collected specimens belonged to the Scarabeidae family, with 217 individuals, while Pompilidae exhibited the highest richness with 39 species. Differences in all three forest types were detected only in Chilopoda through similarity analysis. Non-metric multidimensional scaling revealed distinctions in both Chilopoda and Scarabeidae. All taxa exhibited changes in community composition. Conclusions: Each group responds differently to disturbance levels. Scarabeidae and Chilopoda demonstrate more favorable characteristics, though other taxa also hold potential for highlighting distinct ecosystem features.
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Aguilar, P., Raven, K., Lamas, G., & Redolfi, I. (1995). Sinopsis de los hexápodos conocidos del Perú. Revista Peruana de Entomología, 37(1), 1–9.

Amaru-Castelo, J., & Marquina-Montesinos, E. (2023). Diversidad de avispas en un gradiente de perturbación de los ecosistemas de la Reserva de Biósfera del Manú (Perú): Su valor bioindicador. Ecología Austral, 33(1), 598–608.

Andersson, P., Koffman, A., Sjödin, N. E., & Johansson, V. (2017). Roads may act as barriers to flying insects: species composition of bees and wasps differs on two sides of a large highway. Nature Conservation, 18(1), 47–59.

Aukema, B. (1995). The Evolutionary Significance of Wing Dimorphism in Carabid Beetles (Coleoptera: Carabidae). Researches on Population Ecology, 37(1), 105–110.

Avendaño-Mendoza, C., Morón-Ríos, A., Cano, E. B., & León-Cortés, J. (2005). Dung beetle community (Coleoptera: Scarabaeidae: Scarabaeinae) in a tropical landscape at the Lachua Region, Guatemala. Biodiversity and Conservation, 14(4), 801–822.

Banks, N. H. (1946). Studies of South American Psammocharidae. Part 1. Bulletin of the Museum of Comparative Zoology, 96(4), 311–525.

Banks, N. H. (1947). Studies of South American Psammocharidae. Part 2. Bulletin of the Museum of Comparative Zoology, 99(2), 370–486.

Baselga, A. (2013). Separating the two components of abundance-based dissimilarity: Balanced changes in abundance vs abundance gradients. Methods in Ecology and Evolution, 4(6), 552–557.

Baselga, A. (2017). Partitioning abundance-based multiple-site dissimilarity into components: balanced variation in abundance and abundance gradients. Methods in Ecology and Evolution, 8(7), 799–808.

Bonato, L., Edgecombe, G., Lewis, J., Minelli, A., Pereira, L., Shelley, R. M., & Zapparoli, M. (2010). A common terminology for the external anatomy of centipedes (Chilopoda). ZooKeys, 69(1), 17–51.

Bowie, M. H., Stokvis, E., Barber, K., Marris, J., & Hodge, S. (2019). Identification of potential invertebrate bioindicators of restoration trajectory at a quarry site in Hunua, Auckland, New Zealand. New Zealand Journal of Ecology, 43(1), 1-11.

Campbell, J., & Hanula, J. (2007). Efficiency of Malaise traps and colored pan traps for collecting flower visiting insects from three forested ecosystems. Journal of Insect Conservation, 11(4), 399-408.

Carignan, V., & Villard, M. (2002). Selecting indicator species to monitor ecological integrity: A review. Environmental Monitoring and Assessment, 78(1), 45–61.

Castro, A. V., Porrini, D. P., & Cicchino, A. C. (2017). Diversidad de Carabidae (Insecta: Coleoptera) en distintos ambientes de un agroecosistema del sudeste bonaerense, Argentina. Ecología Austral, 27(2), 252–265.

Catenazzi, A., Lehr, E., & May, R. (2013). The amphibians and reptiles of Manu National Park and its buffer zone, Amazon basin and eastern slopes of the Andes, Peru. Biota Neotropical, 13(4), 269-283.

Chowdhury, S., Dubey, V. K., Choudhury, S., Das, A., Jeengar, D., Sujatha, B., Kumar, A., Kumar, N., Semwal, A., & Kumar, V. (2023). Insects as bioindicator: A hidden gem for environmental monitoring. Frontiers in Environmental Science, 11, 273.

Corro, P., & Cambra, R. (2011). Diversidad De Avispas (Hymenoptera: Pompilidae) cazadoras de arañas del Parque Nacional Darién, República De Panamá. Tecnociencia, 13(1), 77–90.

Cuellar-Cardozo, J. A., Castro-Rebolledo, M. I., & Jaramillo, M. A. (2020). Diversidad y composición de Odonata asociadas con diferentes condiciones de la vegetación riparia a lo largo de un arroyo en Paicol-Huila, Colombia. Actualidades Biológicas, 42(113), 1–11.

Cupul-Magaña, F. G. (2011). Guía para la determinación de las familias de Cienpiés (Myriapoda: Chilopoda) de México. Revista Bio Ciencias, 4(1), 40-51.

Cupul-Magaña, F. G. (2014). Los ciempiés escolopendromorfos (Chilopoda: Scolopendromorpha) de México: clave para géneros. Revista Colombiana de Entomologia, 40(2), 286–291.

Cupul-Magaña, F., & Flores-Guerrero, U. (2016). Guía para la identificación de las familias de ciempiés (Myriapoda: Chilopoda) de México: una actualización. Revistas Bio Ciencias, 4(1), 40–51.

Dourojeanni, M. J. (2019). Conservación de insectos en la Amazonia. Ecología Aplicada, 18(2), 189–202.

Duelli, P., Obrist, M. K., & Schmatz, D. R. (1999). Biodiversity evaluation in agricultural landscapes: Above-ground insects. Agriculture, Ecosystems and Environment, 74(1), 33–64.

Edmons, W. D., & Zidek, J. (2004). Revision of the Neotropical Dung Beetle Genus Oxysternon (Scarabeidae: Scarabeinae: Phanaeni). Folia Heyrovskyana, 11(1), 1–58.

Edmonds, W. D., & Zidek, J. (2010). A taxonomic review of the neotropical genus Coprophanaeus Olsoufieff, 1924 (Coleoptera: Scarabaeidae, Scarabaeinae). Insecta Mundi, 129(1), 1–116.

Edmonds, W. D., & Zídek, J. (2012). Taxonomy of Phanaeus revisited: Revised keys to and comments on species of the New World dung beetle genus Phanaeus Macleay, 1819 (Coleoptera: Scarabeidae: Scarabeinae: Phanaeini). Insecta Mundi, 274(1), 1–110.

Erwin, T. L. (1991). Natural history of the carabid beetles at the BIOLAT Biological Station, Rio Manu, Pakitza, Peru. Revista peruana de entomología, 33(1), 1–85.

Evans, H. E. (1965). Studies on neotropical Pompilidae (Hymenoptera). I. The genus Agenioideus Ashmead in South America. Breviora, 234(1), 1–7.

Evans, H. E. (1966). Studies on Neotropical Pompilidae (Hymenoptera). II. Genus Aridestus Banks. Psyche, 73(2), 116–122.

Evans, H. E. (1969). Studies on Neotropical Pompilidae (Hymenoptera). V. Austrochares Banks. Psyche, 76(1), 18–28.

Evans, H. E. (1973). Studies on Neotropical Pompilidae (Hymenoptera) IX. The genera of Auplopodini. Psyche, 80(1), 212–226.

Favila, M., & Halffter, G. (1997). The use of indicator groups for measuring biodiversity as related to community structure and function. Acta Zoológica Mexicana, 72(1), 1–25.

Fernández, F. (2000). Avispas Cazadoras de Arañas (Hymenoptera: Pompilidae) de la Región Neotropical. Biota Colombiana, 1(1), 3–24.

Fernández, F. (2006). Capítulo 53. Familia Pompilidae. In F. Fernández & M. J. Sharkey (Eds.), Introducción a los Hymenoptera de la región Neotropical (pp. 563–575).

Fischer, J., & Lindemayer, D. (2007). Landscape modification and habitat fragmentation: a synthesis. Global Ecology and Biogeography, 16, 265–280.

Gallice, G. R., Larrea-Gallegos, G., & Vázquez-Rowe, I. (2019). The threat of road expansion in the Peruvian Amazon. ORYX, 53(2), 284–292.

García-Ruiz, A. (2003). Ecología de las comunidades de Quilópodos en áreas modificadas por depósito de residuos sólidos urbanos inertes. Ecologia, 17(1), 191–197.

Gardner, T. A., Hernández, M. I., Barlow, J., & Peres, C. A. (2008). Understanding the biodiversity consequences of habitat change: the value of secondary and plantation forests for neotropical dung beetles. Journal of applied ecology, 45(3), 883-893.

Genier, F. (1996). A revision of the Neotropical genus Ontherus Erichson (Coleoptera: Scarabeidae, Scarabeinae). Memoirs of the Entomological Society of Canada, 170(170), 1–169.

Genier, F. (2009). Le Genre Eurysternus Dalman 1824 (Scarabaeidae: Scarabaeinae: Oniticellini) révision taxonomique et clés de détermination illustrées. Pensoft publishers.

Génier, F. (2012). Article A new species and notes on the subgenus Deltochilum (Deltochilum) Eschscholtz, 1822 (Coleoptera: Scarabaeidae: Scarabaeinae: Deltochilini). Zootaxa, 3357, 25–36.

Gerhardt, A. (2002). Bioindicator species and their use in biomonitoring. Environmental monitoring, 1, 77-123.

Gerlach J., Samways, M., & Pryke, J. (2013). Terrestrial invertebrates as bioindicators: an overview of available taxonomic groups. Journal of insect conservation, 17, 831-850.

Gómez-Ruiz, P., Tapia-Sedeña, A., Ramírez-García, B., Pinho, B., & Arroyo-Rodríguez, V. (2016). Diferenciación florística a lo largo de un gradiente de perturbación antrópica en un paisaje fragmentado. The Mexican Naturalist, 7(1), 1–5.

González-Alvarado, A., & Vaz-De-Mello, F. Z. (2014). Taxonomic review of the subgenus Hybomidium Shipp 1897 (Coleoptera: Scarabaeidae: Scarabaeinae: Deltochilum). Annales de la Societe Entomologique de France, 50(1), 431-476.

Granados, J. M., Kohlmann, B., & Russo, R. (2010). Escarabajos del estiércol como bioindicadores del impacto ambiental causado por cultivos en la región Atlántica de Costa. Tierra Tropical, 6(2), 181–189.

Grootaert, P., Pollet, M., Dekoninck, W., & Van-Achterberg, C. (2010). Chapter 15. Sampling insects: general techniques, strategies and remarks. In Eymann, J., Degreef, J., Hāuser, J. Monje, C., Samyn, Y. and Vanden Spiegel, D. (Eds.), Manual on Field Recording Techniques and Protocols for All Taxa Biodiversity Inventories and Monitoring (pp. 337-399). Abc Taxa, Belgium.

Hill, M. O. (1973). Diversity and Eveness: A unifying notation and Its consequences. Ecology, 54(2), 427–432.

Kumar, A., & Ram, J. (2005). Anthropogenic disturbances and plant biodiversity in forests of Uttaranchal, central Himalaya. Biodiversity and Conservation, 14(1), 309–331.

Legendre, P., & Legendre, L. (1983). Numerical Ecology. Elsevier Science.

Lira-Torres, I. (2006). Abundancia, densidad, preferencia de hábitat y uso local de los vertebrados en la Tuza de Monoy, Santiago Jamiltepec, Oaxaca. Revista Mexicana de Mastozoología, 10(1), 41-66.

Lövei, G., & Sunderland, K. (1996). Ecology and behaviour of ground beetles (Coleoptera: Carabidae). Annual Review of Entomology, 41, 231-256.

Márquez, J. (2005). Técnicas de colecta y preservación de insectos. Boletín Sociedad Entomológica Aragonesa, 37, 385–408.

Más-Martínez, R.; Fernández-Denis, I., Villegas, R., & Bautista, F. (2011). 8. Monolitos de Suelo. In F. Bautista-Zúñiga (Eds.), Técnicas de muestreo para manejadores de recursos naturales (pp. 259-274). Universidad Nacional Autónoma de México.

McDonald, J. (2014). Handbook of Biological Statistics. University of Delaware.

McGeoch, M. A., Van Rensburg, B. J., & Botes, A. (2002). The verification and application of bioindicators: a case study of dung beetles in a savanna ecosystem. Journal of applied ecology, 39(4), 661-672.

Mei, Z., Scheper, J., Bommarco, R., de Groot, G. A., Garratt, M. P. D., Hedlund, K., Potts, S. G., Redlich, S., Smith, H. G., Steffan-Dewenter, I., van der Putten, W. H., van Gils, S., & Kleijn, D. (2023). Inconsistent responses of carabid beetles and spiders to land-use intensity and landscape complexity in north-western Europe. Biological Conservation, 283.

Missa, O., Basset, Y., Alonso, A., Miller, S. E., Curletti, G., De Meyer, M., Eardley, C., & Wagner, T. (2009). Monitoring arthropods in a tropical landscape: relative effects of sampling methods and habitat types on trap catches. Journal of Insect conservation, 13, 103-118

Moritz, C., Richardson, K. S., Ferrier, S., Monteith, G. B., Stanisic, J., Williams, S. E., & Whiffin, T. (2001). Biogeographical concordance and efficiency of taxon indicators for establishing conservation priority in a tropical rainforest biota. Proceedings of the Royal Society B, 268(1479), 1875–1881.

Myers, N., Mittermeier, R. A., Mittermeier, C. G., Da Fonseca, G., & Kent, J. (2000). Biodiversity hotspots for conservation priorities. NATURE, 403(1), 853–858.

Nichols, E., Larsen, T., Spector, S., Davis, A. L., Escobar, F., Favila, M., & Vulinec, K. (2007). Global dung beetle response to tropical forest modification and fragmentation: a quantitative literature review and meta-analysis. Biological conservation, 137(1), 1-19.

Nielsen, T. S. (2007). Deforestation and biodiversity: effects of bushland cultivation on dung beetles in semi-arid Tanzania. Biodiversity and Conservation, 16(1), 2753-2769.

Niemelä, J. (2000). Biodiversity monitoring for decision-making. Annales Zoologici Fennici, 37(4), 307–317.

Niemelä, J. (2001). Carabid beetles (Coleoptera: Carabidae) and habitat fragmentation: A review. European Journal of Entomology, 98(2), 127–132.

Noonan, G. (1981a). South American species of the subgenus Anisotarsus Chaudoir (genus Notiobia Perty: Carabidae: Coleoptera). Part I: Taxonomy and Natural History. Milwaukee Public Museum. Estados Unidos.

Noonan, G. (1981b). South American species of the subgenus Anisotarsus Chaudoir (genus Notiobia Perty: Carabidae: Coleoptera) Part II: Evolution and Biogeography. Milwaukee Public Museum. Estados Unidos.

Noriega, J. A., March‐Salas, M., Castillo, S., García‐Q, H., Hortal, J., & Santos, A. M. (2021). Human perturbations reduce dung beetle diversity and dung removal ecosystem function. Biotropica, 53(3), 753-766.

Patterson, B., Stotz, D., & Solari, S. (2006). Mammals and Birds of the Manu. Biosphere Reserve, Peru. Fieldiana Zoology, 110(1): 1-5.[1:MABOTM]2.0.CO;2

Pearson, D. (1984). The tiger Beetles (Coleoptera: Cicindelidae) of the Tambopata Reverved Zone, Madre de Dios, Perú. Revista Peruana de entomología, 27(1), 15–24.

Pradesh, A., Bhuyan, P., Khan, M. L., & Tripathi, R. S. (2003). Tree diversity and population structure in undisturbed and human-impacted stands of tropical wet evergreen forest in Arunachal Pradesh, Eastern Himalayas, India. Biodiversity and Conservation, 12(1), 1753–1773.

Parmar, T. K., Rawtani, D., & Agrawal, Y. K. (2016). Bioindicators: The natural indicator of environmental pollution, Frontiers in Life Science, 9(2), 110-118.

Reichardt, H. (1967). A monographic revision of the American Galeritini (Coleoptera, Carabidae). Arquivos de Zoologia, 15(1), 1–176.

Reichardt, H. (1977). A synopsis of the genera of neotropical Carabidae (Insecta: Coleoptera). Quaestiones Entomologicae, 13(1), 346–493.

Reyes-Novelo, E., Delfín-González, H., & Morón, M. Á. (2007). Copro-necrophagous beetle (Coleoptera: Scarabaeidae) diversity in an agroecosystem in Yucatan, Mexico. Revista de Biologia Tropical, 55(1), 83-99.

Rivalier, E. (1969). Démembrement du gnre Odontochila [ Col. Cicindelidae] et révisions des principales epéces. Annales de La Société Entomologique de France, 5(1), 196–239.

Roig Alsina, A. (1984). Contribución al conocimiento de los Pepsinae sudamericanos. II. El género Adirostes Banks (Hymenoptera, Pompilidae). Revista de la Sociedad Entomológica Argentina, 43(1), 165–170.

Roig-Juñet, S., & Dominguez, M. C. (2001). Diversidad de la familia Carabidae (Coleoptera) en Chile. Revista Chilena de Historia Natural, 74(3), 549–571.

Rosenberg, D. K., Noon, B. R., & Charles Meslow, E. (1997). Biological Corridors: Form, Function, and Efficacy. BioScience, 47(10), 677–687.

Salas-Lopez, A., Violle, C., Mallia, L., & Orivel, J. (2017). Land-use change effects on the taxonomic and morphological trait composition of ant communities in French Guiana. Insect Conservation and Diversity, 11(2), 162-173.

SERNAMP. (2016). Áreas naturales protegidas del Perú (2011-2015). Conservación para el desarrollo sostenible. Ministerio del Ambiente. Lima. Perú

Silva, F. A. B., & Valois, M. (2019). A taxonomic revision of the genus Scybalocanthon Martínez, 1948 (Coleoptera: Scarabaeidae: Scarabaeinae: Deltochilini). Zootaxa, 4629 (3), 301-341.

Silva, F. A. B., Louzada, J., & Vaz-De-Mello, F. (2015). A revision of the Deltochillum subgenus Aganhyboma Kolbe, 1893 (Coleoptera: Scarabaeidae: Scarabaeinae). Zootaxa, 3925(4), 451–504.

Spector, S. (2006). Scarabaeine Dung Beetles (coleoptera: Scarabaeidae: Scarabaeinae): An Invertebrate Focal Taxon for Biodiversity Research and Conservation. The Coleopterists Bulletin, 60(5), 71–83.[71:sdbcss];2

Straneo, S. L. (1979). Notes about Classification of the South American Pterostichini with a key for determination of subtribes, genera and subgenera (Coleoptera: Carabidae). Quaestiones Entomologicae, 15(1), 345-356.

Umair Sial, M., Zeeshan Majeed, M., Atiq, A., Farooq, T., Aatif, H. M., Jaleel, W., Khan, S., Akbar, R., Zaman, M., Saeed, R., Ali, Y., Saleh, M., Ullah, F., Ali Khan, K., & Ghrmah, H. A. (2022). Differential efficacy of edaphic traps for monitoring arthropods diversity in subtropical regions. Journal of King Saud University - Science, 34(1), 1-7.

Vanoye-Eligio, M., Meléndez-Ramírez, V., Ayala-Barajas, R., Delfín-González, H., & Horta-Vega, J. V. (2019). Diversity of predatory wasps in two types of vegetation of the State of Yucatán in Mexico. Revista Mexicana de Biodiversidad, 90(2019), 1-11.

Vaz-De-Mello, F. Z., Edmonds, W. D., Ocampo, F. C., & Schoolmeesters, P. (2011). A multilingual key to the genera and subgenera of the subfamily Scarabaeinae of the New World (Coleoptera: Scarabaeidae). Zootaxa, 73(2854), 1-73.

Vitolo, A. L. (2004). Guía para la identificación de los escarabajos tigre (Coleoptera: Cicindelidae) de Colombia. Instituto de investigación de recursos biológicos Alexander Von Humboldt. Ed., Colombia.

Voigtländer, K. (2011). Chilopoda - Ecology. In A. Minelli (Ed.), Treatise on Zoology -Anatomy, Taxonomy, Biology. The Myriapoda (pp. 1–546). Brill Academic publishers.

Whitworth, A., Villacampa, J., Brown, A., Huarcaya, R. P., Downie, R., & MacLeod, R. (2016). Past human disturbance effects upon biodiversity are greatest in the canopy; A case study on rainforest butterflies. PLoS ONE, 11(3), 1-20.


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