Abstract
Forestry companies have replaced and fragmented the native landscapes, generating a large number of unpaved roads, which can have a negative effect on non-flying invertebrates. Polynoncus bullatus is a common necrophagous beetle species depend on fox scats present on unpaved roads in fragmented landscapes in central Chile. Here, the effect of different habitat types (native forest, clear-cuts and unpaved roads) on the abundance of Lycalopex culpaeus scats as well as abundance and survival of P. bullatus in the fragmented landscape was evaluated. Scats and beetles were counted in seven independent fragments during 6 months and through sampling transects. Both responses and factors were associated with GLM, whereas survival was evaluated with a Kaplan-Meier test. Higher scats abundance was found on unpaved roads than other habitat types. Higher P. bullatus abundance was also significantly associated with unpaved roads than clear-cuts and native forest fragments. An additive model between habitat type and scat abundance was correlated with beetle abundance. Survival was significantly lower in unpaved roads, generating up to 42 % of beetles road-killed. Lycalopex culpaeus response positively to fragmentation defecating more on unpaved roads because foxes use it to move through the landscape. This fact attracts more P. bullatus individuals, being run-over by cars and trucks, representing an ecological trap for beetles. This interaction can be predictable and modeled for any period, length or road type avoiding potential massive road-kill events.
Implications for insect conservation. Common and threatened invertebrate species are run-over when minor roads cross valuable natural or protected areas, evidencing the need of advance in road designs compatible with their conservation and mitigating negative impacts of forestry.
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Arévalo JE, Honda W, Arce-Arias A, Häger A (2017) Spatiotemporal variation of roadkills show mass mortality events for amphibians in a highly trafficked road adjacent to a national park, Costa Rica. Rev Biol Trop 65:1261–1276. https://doi.org/10.15517/rbt.v65i4.27903
Baine M, Howard M, Taylor E, James J, Velasco A, Grandas Y, Hartnoll R (2007) The development of management options for the black land crab (Gecarcinus ruricola) catchery in the San Andres Archipelago, Colombia. Ocean Coast Manag 50:564–589. https://doi.org/10.1016/j.ocecoaman.2007.02.007
Barbero E, Palestrini C, Rolando A (1999) Dung beetle conservation: effects of habitat and resource selection (Coleoptera: Scarabaeoidea). J Insect Conserv 3:75–84. https://doi.org/10.1023/A:1009609826831
Baxter-Gilbert JH, Riley JL, Neufeld CJ, Litzgus JD, Lesbarrères D (2015) Road mortality potentially responsible for billions of pollinating insect deaths annually. J Insect Conserv 19:1029–1035. https://doi.org/10.1007/s10841-015-9808-z
Bourg A, Escobar F, MacGregor-Fors I, Moreno CE (2016) Got dung? Resource selection by dung beetles in Neotropical forest fragments and cattle pastures. Neotrop Entomol 45:490–498. https://doi.org/10.1007/s13744-016-0397-7
Burnham KP, Anderson DR (1998) Model selection and inference: a practical information-theoretic approach. Springer-Verlag, New York
Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretical approach. Springer, New York
Bustamante RO, Simonetti JA, Mella JE (1992) Are foxes legitimate and efficient seed dispersers? A field test. Acta Oecol 13:203–208
Cicort-Lucaciu A, Sas-Kovács I, Covaciu-Marcov SD (2016) Non road human influence upon road mortality on three secondary roads in the Vâlsan River protected area, Romania. Oltenia J Stud Nat Sci 32:99–106
Ciolan E, Cicort-Lucaciu A, Sas-Kovács I, Ferenţi S, Covaciu-Marcov SD (2017) Wooded area, forest road-killed animals: Intensity and seasonal differences of road mortality on a small, newly upgraded road in western Romania. Transport Res D-Tr E 55:12–20. https://doi.org/10.1016/j.trd.2017.06.014
Correa C, Puker A, Korasaki V, Ferreira KR (2013) Omorgus suberosus and Polynoncus bifurcatus (Coleoptera: Scarabaeoidea: Trogidae) in exotic and native environments of Brazil. Zoologia (Curitiba) 30:238–241. https://doi.org/10.1590/S1984-46702013000200015
Curtis J (1845) XXIX. Descriptions &c. of the Insects collected by Captain P. P. King R.N. F.R.S. & L.S. in the Survey of the Straits of Magellan.. Trans Linn Soc Lond 19(4):441–475. https://doi.org/10.1111/j.1096-3642.1842.tb00371.x
Curtis PG, Slay CM, Harris NL, Tyukavina A, Hansen MC (2018) Classifying drivers of global forest loss. Science 361:1108–1111. https://doi.org/10.1126/science.aau3445
D'Amico M, Román J, de los Reyes L, Revilla E (2015) Vertebrate road-kill patterns in Mediterranean habitats: who when and where. Biol Conserv 191:234–242. https://doi.org/10.1016/j.biocon.2015.06.010
Diéguez VM, Gómez RS (2004) Aporte al conocimiento de las Trogidae (Coleoptera) de la Argentina. Rev Soc Entomol Arg 63:92–95
Dwernychuk LW, Boag DA (1972) Ducks nesting in association with gulls: an ecological trap? Canadian J Zool 50:559–563. https://doi.org/10.1139/z72-076
Dunn RR, Danoff-Burg JA (2007) Road size and carrion beetle assemblages in a New York forest. J Insect Conserv 11:325–332. https://doi.org/10.1007/s10841-006-9047-4
Epstein R, Weintraub A, Sapunar P, Nieto E, Sessions JB, Sessions J, Bustamante F, Musante H (2006) A combinatorial heuristic approach for solving real-size machinery location and road design problems in forestry planning. Oper Res 54(6):1017–1027. https://doi.org/10.1287/opre.1060.0331
Fabrizio M, Di Febbraro M, Loy A (2019) Where will it cross next? Optimal management of road collision risk for otters in Italy. J Environ Manag 251:109609. https://doi.org/10.1016/j.jenvman.2019.109609
González-Hernández AL, Navarrete-Heredia JL, Quiroz-Rocha GA, Deloya C (2015) Coleópteros necrócolos (Scarabaeidae: Scarabaeinae, Silphidae y Trogidae) del Bosque Los Colomos, Guadalajara, Jalisco, México. Rev Mex Biodiv 86:764–770. https://doi.org/10.1016/j.rmb.2015.07.006
Grez AA (2005) El valor de los fragmentos pequeños del bosque maulino en la conservación de la fauna de coleópteros epigeos. In: Smith-Ramírez C, Armesto J, Valdovinos C (eds) Biodiversidad y ecología de los bosques de la cordillera de la Costa de Chile. Editorial Universitaria, Santiago, pp 565–572
Guerrero C, Espinoza L, Niemeyer HM, Simonetti JA (2006) Using fecal profiles of bile acids to assess habitat use by threatened carnivores in the Maulino forest of central Chile. Rev Chi Hist Nat 79:89–95. https://doi.org/10.4067/S0716-078x2006000100008
Haddad NM, Brudvig LA, Clobert J, Davies KF, Gonzalez A, Holt RD, Lovejoy TE, Sexton JO, Austin MP, Collins CD, Cook WM, Damschen EI, Ewers RM, Foster BL, Jenkins CN, King AJ, Laurance WF, Levey DJ, Margules CR, Melbourne BA, Nicholls AO, Orrock JL, Song D-X, Townshend JR (2015) Habitat fragmentation and its lasting impact on Earth’s ecosystems. Sci Adv 1(2):e1500052. https://doi.org/10.1126/sciadv.1500052
Hayward MW, Hayward GJ, Kerley GIH (2010) The impact of upgrading roads on the conservation of the threatened flightless dung beetle, Circellum bacchus (F.) (Coleoptera: Scarabaeidae). Coleopt Bull 64(1):75–80. https://doi.org/10.1649/0010-065X-64.1.75
Hedin J, Isacsson G, Jonsell M, Komonen A (2008) Forest fuel piles as ecological traps for saproxylic beetles in oak. Scan J For Res 23:348–357. https://doi.org/10.1080/02827580802269991
Horváth G, Malik P, Kriska G, Wildermuth H (2007) Ecological traps for dragonflies in a cemetery: the attraction of Sympetrum species (Odonata: Libellulidae) by horizontally polarizing black gravestones. Freshw Biol 52:1700–1709. https://doi.org/10.1111/j.1365-2427.2007.01798.x
Kaplan EL, Meier P (1958) Nonparametric estimation from incomplete observations. J Am Stat Assoc 53:457–481
Keilsohn W, Narango DL, Tallamy DW (2018) Roadside habitat impacts insect traffic mortality. J Insect Conserv 22:183–188. https://doi.org/10.1007/s10841-018-0051-2
Kang W, Minor ES, Woo D, Lee D, Park CR (2016) Forest mammal roadkills as related to habitat connectivity in protected areas. Biodiv Conserv 25:2673–2686. https://doi.org/10.1007/s10531-016-1194-7
Lehtonen TK, Babic NL, Piepponen T, Valkeeniemi O, Borshagovski AM, Kaitala A (2021) High road mortality during female-biased larval dispersal in an iconic beetle. Behav Ecol Sociobiol 75:1–10. https://doi.org/10.1007/s00265-020-02962-6
Lomolino MV, Creighton JC, Schnell GD, Certain DL (1995) Ecology and conservation of the endangered American burying beetle (Nicrophorus americanus). Conserv Biol 9:605–514. https://doi.org/10.1046/j.1523-1739.1995.09030605.x
Martensen AC, Pimentel RG, Metzger JP (2008) Relative effects of fragment size and connectivity on bird community in the Atlantic Rain Forest: implications for conservation. Biol Conserv 141:2184–2192. https://doi.org/10.1016/j.biocon.2008.06.008
Ministerio del Medio Ambiente de Chile (2021) Clasificación según estado de conservación. Ministerio del Medio Ambiente de Chile. http://www.mma.gob.cl/clasificacionespecies/index.htm. Accessed 15 April 2021
Miranda A, Altamirano A, Cayuela L, Lara A, González M (2017) Native forest loss in the Chilean biodiversity hotspot: revealing the evidence. Reg Environ Change 17:285–297. https://doi.org/10.1007/s10113-016-1010-7
Moreira-Arce D, Vergara PM, Boutin S, Simonetti JA, Briceño C, Acosta-Jamett G (2015a) Native forest replacement by exotic plantations triggers changes in prey selection of mesocarnivores. Biol Conserv 192:258–267. https://doi.org/10.1016/j.biocon.2015.09.015
Moreira-Arce D, Vergara PM, Boutin S (2015b) Diurnal human activity and introduced species affect occurrence of carnivores in a human-dominated landscape. PloS ONE 10(9):e0137854. https://doi.org/10.1371/journal.pone.0137854
Moreira-Arce D, Vergara PM, Boutin S, Carrasco G, Briones R, Soto GE, Jimenez JE (2016) Mesocarnivores respond to fine-grain habitat structure in a mosaic landscape comprised by commercial forest plantations in southern Chile. Forest Ecol Manag 369:135–143. https://doi.org/10.1016/j.foreco.2016.03.024
Muñoz F, Huerta A, Curkovic T (2021) Diversidad de coleópteros epigeos en bosques de Nothofagus glauca y plantaciones de Pinus radiata en Chile central. Rev Colomb Entomol 47(1):e7522. https://doi.org/10.25100/socolen.v47i1.7522
Muñoz PT, Torres FP, Megías AG (2015) Effects of roads on insects: a review. Biodiv Conserv 24:659–682. https://doi.org/10.1007/s10531-014-0831-2
Pliscoff P, Simonetti JA, Grez AA, Vergara PM, Barahona-Segovia RM (2020) Defining corridors for movement of multiple species in a forest-plantation landscape. Glob Ecol Conserv 23:e01108. https://doi.org/10.1016/j.gecco.2020.e01108
R Development Core Team (2019) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. Available form: http://www.R-project.org [Accessed 15 Sep 2016]
Poch TJ, Simonetti JA (2013) Insectivory in Pinus radiata plantations with different degree of structural complexity. For Ecol Manag 304:132–136. https://doi.org/10.1016/j.foreco.2013.04.044
Ramirez-Collio K, Vergara PM, Simonetti JA (2017) Converting clear cutting into a less hostile habitat: the importance of understory for the abundance and movement of the Chestnut-throated Huet-Huet (Pteroptochos castaneus: Rhinocryptidae). For Ecol Manag 384:279–286. https://doi.org/10.1016/j.foreco.2016.11.005
Ries L, Fagan WF (2003) Habitat edges as a potential ecological trap for an insect predator. Ecol Entomol 28:567–572. https://doi.org/10.1046/j.1365-2311.2003.00550.x
Russo LF, Barrientos R, Fabrizio M, Di Febbraro M, Loy A (2020) Prioritizing road-kill mitigation areas: a spatially explicit national‐scale model for an elusive carnivore. Divers Distrib 26:1093–1103. https://doi.org/10.1111/ddi.13064
Ryu M, Kim JG (2021) Coastal road mortality of land crab during spawning migration. Sci Rep 11:1–8. https://doi.org/10.1038/s41598-021-86143-z
Seibert HC, Conover JH (1991) Mortality of vertebrates and invertebrates on an Athens County, Ohio, highway. Ohio J Sci 91:163–166
Seshadri KS, Ganesh T (2011) Faunal mortality on roads due to religious tourism across time and space in protected areas: a case study from south India. Forest Ecol Manag 262:1713–1721. https://doi.org/10.1016/j.foreco.2011.07.017
Strümpher WP, Farrell J, Scholtz CH (2014) Trogidae (Coleoptera: Scarabaeoidea) in forensic entomology: occurrence of known and new species in Queensland, Australia. Austral Entomol 53:368–372. https://doi.org/10.1111/aen.12084
Teodor LA, Ferenţi S, Covaciu-Marcov SD (2019) Weevils die in vain? Understanding messages from road-killed weevils (Coleoptera: Curculionoidea). Coleop Bull 73:359–368. https://doi.org/10.1649/0010-065X-73.2.359
Verdugo A (2014) Morfología de los estadios inmaduros, biología y comportamiento de Trox cotodognanensis Compte, 1986 en Cádiz (Coleoptera: Scarabaeoidea: Trogidae). Rev Gaditana Entomol 5:211–224
Vergara PM, Simonetti JA (2004) Avian responses to fragmentation of the Maulino Forest in central Chile. Oryx 38(4):383–388. https://doi.org/10.1017/S0030605304000742
Wintle BA, Kujala H, Whitehead A, Cameron A, Veloz S, Kukkala A, Moilanen A, Gordon A, Lentini PA, Cadenhead NCR, Bekessy SA (2019) Global synthesis of conservation studies reveals the importance of small habitat patches for biodiversity. Proc Nat Acad Sci 116:909–914. https://doi.org/10.1073/pnas.1813051115
Yamada Y, Sasaki H, Harauchi Y (2010a) Composition of road-killed insects on coastal roads around Lake Shikotsu in Hokkaido, Japan. J Rakuno Gakuen Univ Nat Sci 34:177–184
Yamada Y, Sasaki H, Harauchi Y (2010) Effects of narrow roads on the movement of carabid beteles (Coleoptera, Carabidae) in Nopporo Forest Park, Hokkaido. J Insect Conserv 14:151–157. https://doi.org/10.1007/s10841-009-9236-z
Acknowledgements
We would like to thank Carlos Reyes and Corporación Nacional Forestal (CONAF) and MASISA for allowing us to work in the Reserva Nacional Los Queules and pine plantations, and Cecilia Smith-Ramírez for her logistic support. I appreciate the valuable comments of Darío Moreira-Arce, Marcelo Lagos, Isaí Madriz and help of Laura Pañinao-Monsálvez. Also, thanks to Peter D. Lewis for English revision. Funding and technical support from the Fondo Nacional de Desarrollo Científico y Tecnológico (FONDECYT) by Grant 1140657 to Javier Simonetti, Audrey Grez, Pablo Vergara and Patricio Pliscoff; postdoctoral Grant 3160037 to André Rubio; CONICYT doctoral scholarship 21160404 and FONDECYT 3200817 to R.M.B.-S. supported this study.
Funding
FONDECYT 1140657; postdoctoral FONDECYT 3160037; CONICYT doctoral scholarship 21160404 and FONDECYT 3200817.
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Barahona-Segovia, R.M. Until death do us part: abundance and survival of necrophagous beetle species associated with fox scats in fragmented landscapes. J Insect Conserv 25, 521–530 (2021). https://doi.org/10.1007/s10841-021-00320-z
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DOI: https://doi.org/10.1007/s10841-021-00320-z