Abstract
The olive ridley sea turtle, Lepidochelys olivacea (Eschscholtz, 1829), nests en masse in the protected natural area of La Escobilla, Mexico. On this beach, Omorgus suberosus (Fabricius, 1775), a sapro-necrophagous beetle, feeds on the sea turtles’ decomposing and live eggs and is considered to be a threat for the conservation of L. olivacea. However, the abundance and reproductive phenology of O. suberosus in relation to the spatial and temporal availability of this food resource are unknown. We tested two alternative hypotheses during the 2013–2014 nesting season of L. olivacea: (i) abundance and female reproductive phenology of beetles are determined by the spatial and temporal availability of decomposing eggs that accumulate during the turtle nesting season, and (ii) abundance and female reproductive phenology of beetles are related to the increase in the concentration of seasonal and/or new turtle nests. Twenty-four plots (1 m2) were sampled in three areas with different turtle nesting densities. Spatially, beetle abundance was greater where turtle nest density was high and decomposed eggs were abundant. At the temporal level, old nests (> 45 days after egg deposition) were abundant and the presence of seasonal and new nests (~ 45 or fewer days after egg deposition) appeared to trigger sexual maturation in female beetles. Immature female beetles were more abundant throughout the turtles’ nesting season, and mature females were only abundant during the turtle arribadas with the highest number of seasonal nests. We conclude that abundance and female reproductive phenology of O. suberosus females are influenced by the quantity and quality of the resource. These findings are useful to understand the interaction of L. olivacea with other species and to strengthen the conservation plans of this turtle species.
Similar content being viewed by others
Data availability
Supplementary material is available in Online resource 1. The raw data used and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Abreu-Grobois A, Plotkin P (2008) IUCN SSC Marine Turtle Specialist Group. Lepidochelys olivacea. The IUCN Red List of Threatened Species 2008: e.T11534A3292503. https://www.iucnredlist.org/species/11534/3292503. Accessed 30 April 2020
Agarwala BK, Yasuda H, Sato S (2008) Life history response of a predatory ladybird, Harmonia axyridis(Pallas) (Coleoptera: Coccinellidae), to food stress. Appl Entomol Zool 43:183–189
Alckmin-Márquez E, Price PW, Cobb NS (2000) Resource abundance and insect herbivore diversity on woody fabaceous desert plants. Environ Entomol 29:696–703
Allgower K (1979) Effect of the Scarab beetle Trox suberosus on the hatching success of the east Pacific green turtle Chelonia mydas agassizi in the Galapagos Islands. Inf An Estac Ci Ch Darwin Santa Cruz 152–154
Baena ML, Escobar F (2016)Omorgus suberosus (hide beetle). CABI International, Invasive Species Compendium, CABI, Wallingford, UK. http://www.cabi.org/isc/datasheet/119100
Baena ML, Escobar F, Halffter G, García J (2015)Omorgus suberosus beetle predation on endangered sea turtle (Lepidochelys olivacea) nests: the effect of spatial distribution and density. PLoS One 10(9):e0139538
Bauerfeind SS, Fischer K (2005) Effects of food stress and density in different life stages on reproduction in a butterfly. Oikos 111:514–524
Bell WJ, Bohm MK (1975) Oosorption in insects. Biol Rev 50:373–396
Bernardo J, Plotkin PT (2007) An evolutionary perspective on the arribada phenomenon and reproductive behavioral polymorphism of olive ridley sea turtles (Lepidochelys olivacea). In: Plotkin PT (ed) Biology and conservation of Ridley sea turtles. Johns Hopkins University Press, Baltimore, pp 58–87
Bézy VS, Valverde RA, Plante CJ (2015) Olive ridley sea turtle hatching success as a function of the microbial abundance in nest sand at Ostional, Costa Rica. PLoS One 10:e0118579
Boggs CL (1997) Reproductive allocation from reserves and income in butterfly species with differing adult diets. Ecology 78:181–191
Booth DT (2003) Composition and energy density of eggs from two species of freshwater turtle with twofold ranges in egg size. Comp Biochem Phys A 134:129–137
Braby MF, Jones RE (1995) Reproductive patterns and resource allocation in tropical butterflies: influence of adult diet and seasonal phenotype on fecundity, longevity and egg size. Oikos 72:189–204
Büning J (1994) The insect ovary. Chapman & Hall, London, p 400
Chmura HE, Kharouba HM, Ashander J, Ehlman SM, Rivest EB, Yang LH (2019) The mechanisms of phenology: the patterns and processes of phenological shifts. Ecol Monogr 89(1):e01337
CONANP (2009) Comisión Nacional de Áreas Naturales Protegidas. Estudio previo justificativo para establecer el área natural protegida en categoría de Santuario Playa de Escobilla, Santa María Tonameca, Oaxaca
CONANP (2011) Comisión Nacional de Áreas Naturales Protegidas. Golfina-procer. Available:http://www.conanp.gob.mx/conanp/dominios/especies/tortugas/sitio/pdf/fichas_tortugas/tortuga_golfina_2011.pdf
Cornelius SE (1986) The Sea Turltes of Santa Rosa National Park. Fundación de Parques Nacionales (No. 33291). San José, Costa Rica, pp 64
Cortez V (2013) Ecología química y perspectivas de su aplicación en la conservación de la biodiversidad. Cuadernos de Biodiversidad 201341:16–21
Cortez V, Verdú JR, Ortiz AJ, Halffter G (2017) Identification and evaluation of semiochemicals for the biological control of the beetle Omorgus suberosus (F.) (Coleoptera: Trogidae), a facultative predator of eggs of the sea turtle Lepidochelys olivacea (Eschscholtz). PLoS One 12(2):e0172015
Crawley MJ (2007) The R book. 1st ed. Chichester UK: John Wiley & Sons Ltd
Danks HV (2007) The elements of seasonal adaptations in insects. Can Entomol 139:1–44
DOF (2010) Diario Oficial de la Federación. Norma Oficial Mexicana NOM-059-SEMARNAT-2010. Protección ambiental-Especies nativas de México de flora y fauna silvestres. Categorías de riesgo y especificaciones para su inclusión, exclusión o cambio. Lista de especies en riesgo. Available:http://dof.gob.mx/nota_detalle.php?codigo=5173091&fecha=30/12/2010
Ellwood ER, Diez JM, Ibánez I, Primack RB, Kobori H, Higuchi H, Silander JA (2012) Disentangling the paradox of insect phenology: are temporal trends reflecting the response to warming? Oecologia 168:1161–1171
Fox J, Weisberg S (2019) An R companion to applied regression, Third edition. Sage, Thousand Oaks https://socialsciences.mcmaster.ca/jfox/Books/Companion/
García E (1981) Modificaciones al Sistema de Clasificación climática de Köppen. Para adaptarlo a las condiciones de la República Mexicana. 3rd ed. Instituto de Geografía, Universidad Nacional Autónoma de México (UNAM)
Harfush M, Ávila J, Ruvalcaba G, López EM (2008) The evident destruction of olive ridley sea turtle eggs (Lepidochelys olivacea) by the beetle Omorgus suberosus (Fabricius, 1775) at Escobilla Beach, Oaxaca: a proposal of a biological control. In: Kalb H, Rohde AS, Gayheart K, Shanker K, editors. Proceedings of the twenty-fifth annual symposium on sea turtle biology. pp. 89–90
Hart DD, Robinson CT (1990) Resource limitation in a stream community: phosphorus enrichment effects on periphyton and grazers. Ecology 71:1494–1502
Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363
Jensen K, Mayntz D, Toft S, Clissold FJ, Hunt J, Raubenheimer D, Simpson SJ, (2012) Optimal foraging for specific nutrients in predatory beetles. Proc R Soc B Biol Sci 279(1736):2212-2218
Kalinová B, Podskalská H, Růžička J, Hoskovec M (2009) Irresistible bouquet of death—how are burying beetles (Coleoptera: Silphidae: Nicrophorus) attracted by carcasses. Naturwissenschaften 96:889–899
Liebhold A, Koenig WD, Bjørnstad ON (2004) Spatial synchrony in population dynamics. Annu Rev Ecol Evol Syst 35:467–490
López-Reyes E, Harfush M (2000) Determination of the percentage of olive ridley (Lepidochelys olivacea) in situ nests that are affected by beetles at Escobilla beach, Mexico. In: Mosier A, Foley A, Brost B, editors. Proceedings of the twentieth annual symposium on sea turtle biology and conservation. pp. 477
López-Reyes EM, Olivera A (1996) Control del escarabajo que destruye los huevos de la tortuga marina. In: Memorias 1er. Encuentro regional sobre investigación y desarrollo costero: Guerrero, Oaxaca y Chiapas. UMAR, POECO, CONACYT, SEMARNAP, CODE. 14–16 de noviembre. Puerto Ángel, Oaxaca
Markow TA, O’Grady P (2008) Reproductive ecology of Drosophila. Funct Ecol 22:747–759
Martínez MI (2002) Técnicas básicas de anatomía microscopía y de morfometría para estudiar los insectos. Boletín de la S.E.A 30:187–195
Moskalik B, Uetz GW (2016) Female feeding history impacts gonad development and reproductive timing in the wolf spider Schizocosa ocreata (Hentz, 1844). J Arachnol 44:171–175
Nielsen AL, Fleischer S, Hamilton GC, Hancock T, Krawczyk G, Lee JC, Ogburn E, Pote JM, Raudenbush A, Rucker A, Saunders M, Skillman VP, Sullivan J, Timer J, Walgenbach J, Wiman NG, Leskey TC (2017) Phenology of brown marmorated stink bug described using female reproductive development. Ecol Evol 7(17):6680-6690
Ocana M, Harfush-Melendez M, Heppell SS (2012) Mass nesting of olive ridley sea turtles Lepidochelys olivacea at La Escobilla, Mexico: linking nest density and rates of destruction. Endanger Species Res 16:45–54
Osawa N (2005) The effect of prey availability on ovarian development and oosorption in the ladybird beetle Harmonia axyridis (Coleoptera: Coccinellidae). Eur J Entomol 102:503–511
Palestrini C, Barbero E, Zunino M (1992) Biology of the preimaginal stages in trogid beetles (Coleoptera): experimental data. Ital J Zool 59:69–71
Papaj DR (2000) Ovarian dynamics and host use. Annu Rev Entomol 45(1):423–448
Papaj DR (2005) Ovarian dynamics in relation to host quality in the walnut-infesting fly, Rhagoletis juglandis. Funct Ecol 19:396–404
Peralta E, Luna MT (2014) Informe técnico final de temporada de anidación 2013–2014 en el Santuario Playa de Escobilla. Informe interno CMT-CONANP
Pruim R, Kaplan DT, Horton NJ (2017) The mosaic package: helping students to ‘think with data’ using R. R J 9(1):77–102 https://journal.r-project.org/archive/2017/RJ-2017-024/index.html
R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/
Ribeiro C, Dickson BJ (2010) Sex Peptide Receptor and Neuronal TOR/S6K Signaling Modulate Nutrient Balancing in Drosophila. Curr Biol 20(11):1000-1005
Root RB (1973) Organization of a plant-arthropod association in simple and diverse habitats: the fauna of collards (Brassica oleracea). Ecol Monogr 43:95–124
Rosano-Hernández M, Deloya C (2002) Interacción entre Trogidos (Coleoptera: Trogidae) y Tortugas marinas (Reptilia: Cheloniidae) en el Pacífico mexicano. Acta Zool Mex (n.s) 87:29–46
Salazar CP, Pérez JV, Padilla EA, Millán RM (1998)Twenty-five years nesting of olive ridley sea turtle Lepidochelys olivacea in Escobilla Beach, Oaxaca, Mexico. In: Eighteenth International Sea Turtle Symposium, pp 27
Sánchez-Carrillo M, Huerta C, Carrillo-Ruiz H, Escobar F (2017) Anatomical description of the reproductive system and maturation states in females of Omorgus suberosus(Fabricius) (Coleoptera: Trogidae). Coleopt Bull 71:137–142
Scholtz CH, Caveney S (1992) Daily biphasic behaviour in keratin-feeding desert trogid beetles in relation to climate. Ecol Entomol 17:155–159
Simons MA, Smith AR (2018) Ovary activation does not correlate with pollen and nectar foraging specialization in the bumblebee Bombus impatiens. PeerJ 6:e4415
Smykal V, Raikhel AS (2015) Nutritional control of insect reproduction. Curr Opin Insect Sci 11:31-38
Southwood TRE (1961) The number of species of insect associated with various trees. J Anim Ecol 30:1–8
Stavert JR, Drayton BA, Beggs JR, Gaskett AC (2014) The volatile organic compounds of introduced and native dung and carrion and their role in dung beetle foraging behaviour. Ecol Entomol 39:556–565
Tribe GD, Burger BV (2011) Olfactory ecology. In: Simmons LW, Ridsdill-Smith TJ (eds) Ecology and evolution of dung beetles. Wiley-Blackwell, Oxford, pp 87–106
Van Emden FL (1948)Trox larva feeding on locust eggs in Somalia. Proc R Entomol Soc 17:145–148
Vaurie PA (1955) Revision of the genus Trox in North America. Bull Am Mus Nat Hist NY 106:1–89
Wheeler D (1996) The role of nourishment in oogenesis. Annu Rev Entomol 41:407–431
Zito P, Sajeva M, Raspi A, Dötterl S (2014) Dimethyl disulfide and dimethyl trisulfide: so similar yet so different in evoking biological responses in saprophilous flies. Chemoecology 24:261–267
Acknowledgments
We thank Manuel Rodríguez Gómez, Director of the Centro Mexicano de la Tortuga, for his support when we were carrying out the fieldwork and for providing access to the arribada monitoring data. We are grateful to Cuauhtemoc Peñaflores Salazar for his support with field logistics and to Erika Peralta Buendía and María Teresa Luna Medina for their support with the fieldwork. The students of the Escobilla music school kindly assisted in checking the sea turtle nests and collecting beetles, and Israel Huesca provided valuable advice on some of the statistical analyses.
Funding
The Consejo Nacional de Ciencia y Tecnología (CONACYT) provided a postgraduate scholarship to the third author MSC (No. 280599).
Author information
Authors and Affiliations
Contributions
MSC, CHC, and FE conceived and designed the study. MSC performed the field study. MSC and CHC performed the dissections in the laboratory. MLB and FE analyzed the data and visualized the results. MLB wrote the manuscript, with contributions from all of the authors.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. The nests and turtle eggs were handled according to the recommendations of the officials of the Mexican Turtle Center.
Additional information
Communicated by: Oliver Hawlitschek
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(DOCX 1085 kb)
Rights and permissions
About this article
Cite this article
Baena, M.L., Crespo, C.H., Carrillo, M.S. et al. Spatiotemporal variation in Lepidochelys olivacea sea turtle nests and their influence on the abundance and reproductive phenology of the sapro-necrophagous beetle Omorgus suberosus. Sci Nat 107, 47 (2020). https://doi.org/10.1007/s00114-020-01704-y
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00114-020-01704-y