Abstract
Numerous studies have demonstrated that entomophagous arthropods use herbivore-induced plant volatile (HIPV) blends to search for their prey or host. However, no study has yet focused on the response of nocturnal predators to volatile blends emitted by prey damaged plants. We investigated the olfactory behavioral responses of the night-active generalist predatory earwig Doru luteipes Scudder (Dermaptera: Forficulidae) to diurnal and nocturnal volatile blends emitted by maize plants (Zea mays) attacked by either a stem borer (Diatraea saccharalis) or a leaf-chewing caterpillar (Spodoptera frugiperda), both suitable lepidopteran prey. Additionally, we examined whether the earwig preferred odors emitted from short- or long-term damaged maize. We first determined the earwig diel foraging rhythm and confirmed that D. luteipes is a nocturnal predator. Olfactometer assays showed that during the day, although the earwigs were walking actively, they did not discriminate the volatiles of undamaged maize plants from those of herbivore damaged maize plants. In contrast, at night, earwigs preferred volatiles emitted by maize plants attacked by D. saccharalis or S. frugiperda over undamaged plants and short- over long-term damaged maize. Our GC-MS analysis revealed that short-term damaged nocturnal plant volatile blends were comprised mainly of fatty acid derivatives (i.e., green leaf volatiles), while the long-term damaged plant volatile blend contained mostly terpenoids. We also observed distinct volatile blend composition emitted by maize damaged by the different caterpillars. Our results showed that D. luteipes innately uses nocturnal herbivore-induced plant volatiles to search for prey. Moreover, the attraction of the earwig to short-term damaged plants is likely mediated by fatty acid derivatives.
Similar content being viewed by others
References
Adnan M, Khan A (2017) Effect of prey density the biology and functional response of Chrysoperla carnea. J Entomol Zool Stud. 5:916–920
Allmann S, Baldwin IT (2010) Insects betray themselves in nature to predators by rapid isomerization of green leaf volatiles. Science 329:1075–1078. https://doi.org/10.1126/science.1191634
Alvarenga CD, Vendramim JD, Cruz I (1996) Efeito do predador Doru luteipes (Scud.) sobre o crescimento populacional de Schizaphis graminum (Rond.) em diferentes genótipos de sorgo. An Soc Entomol 25:137–140. https://doi.org/10.1590/S1519-566X2002000100018
Ardanuy A, Albajes R, Turlings TC (2016) Innate and learned prey-searching behavior in a generalist predator. J Chem Ecol 42:497–507. https://doi.org/10.1007/s10886-016-0716-9
Arimura GI, Köpke S, Kunert M, Volpe V, David A, Brand P, Dabrowska P, Maffei ME, Boland W (2008) Effects of feeding Spodoptera littoralis on lima bean leaves: IV. Diurnal and nocturnal damage differentially initiate plant volatile emission. Plant Physiol 146:965–973. https://doi.org/10.1104/pp.105.071993
Boos S, Meunier J, Pichon S, Kölliker M (2014) Maternal care provides antifungal protection to eggs in the European earwig. Behav Ecol 25:754–761. https://doi.org/10.1093/beheco/aru046
Bukovinszky T, Poelman EH, Kamp A, Hemerik L, Prekatsakis G, Dicke M (2012) Plants under multiple herbivory: consequences for parasitoid search behaviour and foraging efficiency. Anim Behav 83:501–509. https://doi.org/10.1016/j.anbehav.2011.11.027
Butnariu AR, Pasini A, Reis FS, Bessa E (2013) Maternal care by the earwig Doru lineare eschs. (Dermaptera: Forficulidae). J Insect Behav 26:667–678. https://doi.org/10.1007/s10905-013-9377-5
Capinera JL (2001) Sugarcane borer. University of Florida, Institute of Food and Agricultural Services http://entnemdept.ufl.edu/creatures/field/sugarcane_borer.htm . Accessed 30 September 2016
Chamberlain K, Khan ZR, Pickett JA, Toshova T, Wadhams LJ (2006) Diel periodicity in the production of green leaf volatiles by wild and cultivated host plants of stemborer moths, Chilo partellus and Busseola fusca. J Chem Ecol 32:565–577. https://doi.org/10.1007/s10886-005-9016-5
Chehab EW, Kaspi R, Savchenko T, Rowe H, Negre-Zakharov F, Kliebenstein D, Dehesh K (2008) Distinct roles of jasmonates and aldehydes in plant-defense responses. PLoS One 3:e1904. https://doi.org/10.1371/journal.pone.0001904
Cruz I (2009) Métodos de criação de agentes entomófagos de Spodoptera frugiperda (J.E. Smith). In: Bueno VHP (ed) Controle biológico de pragas: produção massal e controle de qualidade. UFLA, Lavras, pp 111–135
Cruz I, Alvarenga CD, Figueiredo PEF (1995) Biologia de Doru luteipes (Scudder) e sua capacidade predatória de ovos de Helicoverpa zea (Boddie). An Soc Entomol Bras 24:273–278
D'Alessandro M, Turlings TCJ (2006) Advances and challenges in the identification of volatiles that mediate interactions among plants and arthropods. Analyst 131:24–32. https://doi.org/10.1039/b507589k
D'auria JC, Pichersky E, Schaub A, Hansel A, Gershenzon J (2007) Characterization of a BAHD acyltransferase responsible for producing the green leaf volatile (Z)-3-hexen-1-yl acetate in Arabidopsis thaliana. Plant J 49:194–207. https://doi.org/10.1111/j.1365-313X.2006.02946.x
De Boer JG, Hordijk CA, Posthumus MA, Dicke M (2008) Prey and non-prey arthropods sharing a host plant: effects on induced volatile emission and predator attraction. J Chem Ecol 34:281–290. https://doi.org/10.1007/s10886-007-9405-z
De Moraes CM, Lewis WJ, Pare PW, Alborn HT, Tumlinson JH (1998) Herbivore-infested plants selectively attract parasitoids. Nature 393:570–573. https://doi.org/10.1038/31219
De Moraes CM, Mescher MC, Tumlinson JH (2001) Caterpillar-induced nocturnal plant volatiles repel conspecific females. Nature 410(6828):577–580. https://doi.org/10.1038/35069058
De Lange ES, Farnier K, Gaudillat B, Turlings TC (2016) Comparing the attraction of two parasitoids to herbivore-induced volatiles of maize and its wild ancestors, the teosintes. Chemoecology 26:33–44. https://doi.org/10.1007/s00049-015-0205-6
Dicke M, Baldwin IT (2010) The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help’. Trends Plant Sci 15:167–175. https://doi.org/10.1016/j.tplants.2009.12.002
Dicke M, Hilker M (2003) Induced plant defences: from molecular biology to evolutionary ecology. Basic Appl Ecol 4:3–14. https://doi.org/10.1078/1439-1791-00129
Dicke M, Sabelis MW, Takabayashi J, Bruni J, Posthumus MA (1990) Plant strategies of manipulating predator-prey interactions through allelochemicals: prospects for application in pest control. J Chem Ecol 16:3091–3118. https://doi.org/10.1007/BF00979614
Dicke M, van Loon JJA (2000) Multitrophic effects of herbivore-induced plant volatiles in an evolutionary context. Entomol Exp Appl 97:237–249. https://doi.org/10.1046/j.1570-7458.2000.00736.X
Dickens JC (1999) Predator–prey interactions: olfactory adaptations of generalist and specialist predators. Agric For Entomol 1:47–54. https://doi.org/10.1046/j.1461-9563.1999.00007.x
Drukker B, Bruin J, Sabelis MW (2000) Anthocorid predators learn to associate herbivore-induced plant volatiles with presence or absence of prey. Physiol Entomol 25:260–265. https://doi.org/10.1046/j.1365-3032.2000.00190.x
Dudareva N, Negre F, Nagegowda DA, Orlova I (2006) Plant volatiles: recent advances and future perspectives. Crit Rev Plant Sci 25:417–440. https://doi.org/10.1080/07352680600899973
Evans KA, Longépé V (1996) The European earwig: getting the best of both worlds? In: Wiley KB (ed) Proceedings of the second international conference on urban pests. Exeter Press, UK, pp 163–167
Greenham K, McClung CR (2015) Integrating circadian dynamics with physiological processes in plants. Nat Rev Genet 16:598–610. https://doi.org/10.1038/nrg4031
Gouinguené S, Degen T, Turlings TC (2001) Variability in herbivore-induced odour emissions among maize cultivars and their wild ancestors (teosinte). Chemoecology 11:9–16. https://doi.org/10.1007/PL00001832
Gouinguené SP, Turlings TC (2002) The effects of abiotic factors on induced volatile emissions in corn plants. Plant Physiol 129:1296–1307. https://doi.org/10.1104/pp.001941
Haile A, Hofsvang T (2001) Survey of lepidopterous stem borer pests of sorghum, maize and pearl millet in Eritrea. Crop Prot 20:151–157. https://doi.org/10.1016/S0261-2194(00)00125-3
Hassell MP, Southwood TRE (1978) Foraging strategies of insects. Annu Rev Ecol Syst 9:75–98
He XZ, Wang Q, Xu J (2008) European earwig as a potential biological control agent of apple leaf-curling midge. N Z Plant Prot 61:343–349
Hoballah ME, Turlings TCJ (2005) The role of fresh versus old leaf damage in the attraction of parasitic wasps to herbivore-induced maize volatiles. J Chem Ecol 31:2003–2018. https://doi.org/10.1007/s10886-005-6074-7
James DG (2003) Synthetic herbivore-induced plant volatiles as field attractants for beneficial insects. Enviro Entomol 32:977–982. https://doi.org/10.1603/0046-225X-32.5.977
Jones RW, Gilstrap FE, Andrews KL (1988) Biology and life tables for the predaceous earwig, Doru taeniatum [Derm.: Forficulidae]. Entomophaga 33:43–54. https://doi.org/10.1007/BF02372312
Karban R, Baldwin IT (1997) Induced responses to herbivory. The University of Chicago Press, Chicago & London
Kessler A, Baldwin IT (2001) Defensive function of herbivore-induced plant volatile emissions in nature. Science 291:2141–2144. https://doi.org/10.1126/science.291.5511.2141
Kessler A, Baldwin IT (2002) Plant responses to insect herbivory: the emerging molecular analysis. Annu Rev Plant Biol 53:299–328. https://doi.org/10.1146/annurev.arplant.53.100301.135207
Kharboutli MS, Mack TP (1993) Effect of temperature, humidity, and prey density on feeding rate of the striped earwig (Dermaptera: Labiduridae). Environ Entomol 22:1134–1139. https://doi.org/10.1093/ee/22.5.1134
Kidd NA, Jervis MA (2005) Population dynamics. In: Jervis MA (ed) Insects as natural enemies. Springer, Dordrecht, pp 435–523
Lamb RJ, Wellingtown G (1975) life history and population characteristics of the European earwig Forficula auricularia (Dermaptera: Forficulidae), at Vancouver, British Columbia. Can Entomol 107:919–924. https://doi.org/10.4039/Ent107819-8
Lamb RJ (1976) Parental behaviour in the Dermaptera with special reference to Forficula auricularia (Dermaptera: Forficulidae). Can Entomol 108:609–619. https://doi.org/10.4039/Ent108609-6
Le Rü B, Makaya Makosso JP (2001) Prey habitat location by the cassava mealybug predator Exochomus flaviventris: olfactory responses to odor of plant, mealybug, plant–mealybug complex, and plant–mealybug–natural enemy complex. J Insect Behav 14:557–572. https://doi.org/10.1023/A:1012254732271
Luginbill P (1928) The fall armyworm. USDA Tech Bull 34:1–91
Maeda T, Takabayashi J, Yano S, Takafuji A (2000) Effects of light on the tritrophic interaction between kidney bean plants, two-spotted spider mites and predatory mites, Amblyseius womersleyi (Acari: Phytoseiidae). Exp Appl Acarol 24:415–425. https://doi.org/10.1023/A:1006449108245
Maeda T, Kishimoto H, Wright LC, James DG (2015) Mixture of synthetic herbivore-induced plant volatiles attracts more Stethorus punctum picipes (Casey) (Coleoptera: Coccinellidae) than a single volatile. J Insect Behav 28:126–137. https://doi.org/10.1007/s10905-015-9489-1
McCormick AC, Unsicker SB, Gershenzon J (2012) The specificity of herbivore-induced plant volatiles in attracting herbivore enemies. Trends plant Sci 17:303–310. https://doi.org/10.1016/j.Tplants.2012.03.012
Meunier J, Kölliker M (2012) parental antagonism and parent-offspring co-adaptation interact to shape family life. Proc R Soc Lond B 279:3981–3988. https://doi.org/10.1098/rspb.2012.1416
Moayeri HRS, Ashouri A, Poll L, Enkegaard A (2007) Olfactory response of a predatory mirid to herbivore induced plant volatiles: multiple herbivory vs. single herbivory. J Appl Entomol 131:326–332. https://doi.org/10.1111/j.1439-0418.2007.01177.x
Molina-Ochoa J, Carpenter JE, Heinrichs EA, Foster JE (2003) Parasitoids and parasites of Spodoptera frugiperda (Lepidoptera: Noctuidae) in the Americas and Caribbean Basin: an inventory. Fla Entomol 86:254–289. https://doi.org/10.1653/0015-4040(2003)086[0254:PAPOSF]2.0.CO;2
Ninkovic V, Al Abassi S, Pettersson S (2001) The influence of aphid-induced plant volatiles on ladybird beetle searching behavior. Biol Control 21:191–195. https://doi.org/10.1006/bcon.2001.0935
Pasini A, Parra JRP, Lopes JM (2007) Dieta artificial para criação de Doru luteipes (Scudder) (Dermaptera: Forficulidae), predador da lagarta-do-cartucho do milho, Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae). Neotrop Entomol 36:308–311. https://doi.org/10.1590/S1519-566X2007000200020
Paré PW, Tumlinson JH (1997a) Induced synthesis of plant volatiles. Nature 385:30–31. https://doi.org/10.1038/385030a0
Paré PW, Tumlinson JH (1997b) De novo biosynthesis of volatiles induced by insect herbivory in cotton plants. Plant Physiol 114:1161–1167. https://doi.org/10.1104/pp.114.4.1161
Parra JRP (2001) Técnicas de criação de insetos para programas de controle biológico. FEALQ, Piracicaba
Peñaflor MFGV, Erb M, Miranda LA, Werneburg AG, Bento JMS (2011a) Herbivore-induced plant volatiles can serve as host location cues for a generalist and a specialist egg parasitoid. J Chem Ecol 37:1304–1313. https://doi.org/10.1007/s10886-011-0047-9
Peñaflor MFGV, Erb M, Robert CAM, Miranda LA, Werneburg AG, Dossi FCA, Turlings TC, Bento JMS (2011b) Oviposition by a moth suppresses constitutive and herbivore-induced plant volatiles in maize. Planta 234:207–215. https://doi.org/10.1007/s00425-011-1409-9
Picanço MC, De Moura MF, Miranda MMM, Gontijo LM, Fernandes FL (2003) Seletividade de inseticidas a D. luteipes (Scudder, 1876) (Dermaptera: Forficulidae) e Cotesia sp. (Hymenoptera: Braconidae) inimigos naturais de Ascia monuste orseis (Godart, 1818) (Lepidoptera: Pieridae). Ciênc Rural 33:183–188. https://doi.org/10.1590/S0103-84782003000200001
Price PW, Bouton CE, Gross P, McPheron BA, Thompson JN, Weis AE (1980) Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annu Rev Ecol Syst 11:41–65. https://doi.org/10.1146/annurev.es.11.110180.000353
Rasmann S, Köllner TG, Degenhardt J, Hiltpold I, Toepfer S, Kuhlmann U, Gershenzon J, Turlings TCJ (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434:732–737. https://doi.org/10.1038/nature03451
Reddy GVP, Holopainen JK, Guerrero A (2002) Olfactory responses of Plutella xylostella natural enemies to host pheromone, larval frass, and green leaf cabbage volatiles. J Chem Ecol 28:131–143. https://doi.org/10.1023/A:1013519003944
Reis LL, Oliveira LJ, Cruz I (1988) Biologia e Potencial de Doru luteipes no controle de Spodoptera frugiperda. Pesqui Agropecu Bras 23:333–342
Rodriguez-Saona C, Vorsa N, Singh AP, Johnson-Cicalese J, Szendrei Z, Mescher MC, Frost CJ (2011) Tracing the history of plant traits under domestication in cranberries: potential consequences on anti-herbivore defences. J Exp Bot 62:2633–2644. https://doi.org/10.1093/jxb/erq466
Rogers ME, Potter DA (2002) Kairomones from scarabaeid grubs and their frass as cues in below-ground host location by the parasitoids Tiphia vernalis and Tiphia pygidialis. Entomol Exp Appl 102:307–314. https://doi.org/10.1046/j.1570-7458.2002.00951.x
Romero-Sueldo GM, Virla EG (2009) Datos biológicos de Doru luteipes (Dermaptera: Forficulidae) en plantaciones de caña de azúcar y consumo de huevos de Diatraea saccharalis (Lepidoptera: Crambidae) en condiciones de laboratorio. Rev Soc Entomol Argent 68:359–363
Scutareanu P, Drukker B, Bruin J, Posthumus MA, Sabelis MW (1997) Volatiles from Psylla-infested pear trees and their possible involvement in attraction of anthocorid predators. J Chem Ecol 23:2241–2260. https://doi.org/10.1023/B:JOEC.0000006671.53045.16
Seidl-Adams I, Richter A, Boomer KB, Yoshinaga N, Degenhardt J, Tumlinson JH (2015) Emission of herbivore elicitor-induced sesquiterpenes is regulated by stomatal aperture in maize (Zea mays) seedlings. Plant Cell Environ 38:23–34. https://doi.org/10.1111/pce.12347
Shiojiri K, Ozawa R, Matsui K, Kishimoto K, Kugimiya S, Takabayashi J (2006) Role of the lipoxygenase/lyase pathway of host-food plants in the host searching behavior of the two parasitoid species, Cotesia glomerata and Cotesia plutellae. J Chem Ecol 32:969–979. https://doi.org/10.1007/s10886-006-9047-6
Shu S, Jones RL (1989) Kinetic effects of a kairomone in moth scales of the European corn borer on Trichogramma nubilale Ertle & Davis (Hymenoptera: Trichogrammatidae). J Insect Behav 2:123–131
Signoretti AGC, Penaflor MFGV, Moreira LSD, Noronha NC, Bento JMS (2012) Diurnal and nocturnal herbivore induction on maize elicit different innate response of the fall armyworm parasitoid, Campoletis flavicincta. J Pest Sci 85:101–107. https://doi.org/10.1007/s10340-011-0397-7
Stout MJ, Workman KV, Bostock RM, Duffey SS (1998) Specificity of induced resistance in the tomato, Lycopersicon esculentum. Oecologia 113:74–81. https://doi.org/10.1007/s004420050355
Sparks AN (1979) A review of the biology of the fall armyworm. Fla Entomol 62:82–87
Sueldo MR, Bruzzone OA, Virla EG (2010) Characterization of the earwig, Doru lineare, as a predator of larvae of the fall armyworm, Spodoptera frugiperda: a functional response study. J Insect Sci 10:38. https://doi.org/10.1673/031.010.3801
Takabayashi J, Sabelis MW, Janssen A, Shiojiri K, van Wijk M (2006) Can plants betray the presence of multiple herbivore species to predators and parasitoids? The role of learning in phytochemical information networks. Adv Ecol Res 21:3–8. https://doi.org/10.1007/s11284-005-0129-7
Tamiru A, Bruce TJ, Woodcock CM, Caulfield JC, Midega CA, Ogol CK, Mayon P, Birkett MA, Pickett JA, Khan ZR (2011) Maize landraces recruit egg and larval parasitoids in response to egg deposition by a herbivore. Ecol Lett 14:1075–1083. https://doi.org/10.1111/j.1461-0248.2011.01674.x
Turlings TCJ, Alborn HT, Loughrin JH, Tumlinson JH (2000) Volicitin, an elicitor of maize volatiles in oral secretion of Spodoptera exigua: isolation and bioactivity. J Chem Ecol 26:189–202. https://doi.org/10.1023/A:1005449730052
Turlings TC, Bernasconi M, Bertossa R, Bigler F, Caloz G, Dorn S (1998b) The induction of volatile emissions in maize by three herbivore species with different feeding habits: possible consequences for their natural enemies. Biol Control 11:122–129. https://doi.org/10.1006/bcon.1997.0591
Turlings TC, Lengwiler UB, Bernasconi ML, Wechsler D (1998a) Timing of induced volatile emissions in maize seedlings. Planta 207:146–152. https://doi.org/10.1007/s004250050466
Turlings TC, Loughrin JH, Mccall PJ, Röse US, Lewis WJ, Tumlinson JH (1995) How caterpillar-damaged plants protect themselves by attracting parasitic wasps. Proc Natl Acad Sci U S A 92:4169–4174. https://doi.org/10.1073/pnas.92.10.4169
Turlings TCJ, Tumlinson JH (1992) Systemic release of chemical signals by herbivore-injured corn. Proc Natl Acad Sci U S A 89:8399–8402
Turlings TC, Tumlinson JH, Lewis WJ (1990) Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250:1251–1253. https://doi.org/10.1126/science.250.4985.1251
van Loon JJA, Vos EW, Dicke M (2000) Orientation behaviour of the predatory hemipteran Perillus bioculatus to plant and prey odours. Entomol Exp Appl 96:51–58. https://doi.org/10.1046/j.1570-7458.2000.00678.x
Vet LEM, Dicke M (1992) Ecology of infochemical use by natural enemies in a tritrophic context. Annu Rev Entomol 37:141–172. https://doi.org/10.1146/annurev.en.37.010192.001041
Vet LEM, Wäckers FL, Dicke M (1990) How to hunt for hiding hosts: the reliability-detectability problem in foraging parasitoids. Neth J Zool 41:202–213. https://doi.org/10.1163/156854291X00144
Wang P, Su J, Ouyang F, Ge F (2015) Orientation behavior of Propylaea japonica toward visual and olfactory cues from its prey–host plant combination. Entomol Exp et Appl 155:162–166. https://doi.org/10.1111/eea.12295
Weiss MJ, McDonald G (1998) European earwig, Forficula auricularia L.(Dermaptera: Forficulidae), as a predator of the redlegged earth mite, Halotydeus destructor (Tucker)(Acarina: Penthaleidae). Aust Entomol 37:183–185. https://doi.org/10.1111/j.1440-6055.1998.tb01569.x
Weissbecker B, van Loon JJA, Dicke M (1999) Electroantennogram responses of a predator, Perillus bioculatus, and its prey, Leptinotarsa decemlineata, to plant volatiles. J Chem Ecol 25:2313–2325. https://doi.org/10.1023/A:1020825924703
Winkler K, Wäckers FL, Kaufman LV, Larraz V, van Lenteren JC (2009) Nectar exploitation by herbivores and their parasitoids is a function of flower species and relative humidity. Biol Control 50:299–306. https://doi.org/10.1016/j.biocontrol.2009.04.009
Yan Z, Wang C (2006) Similar attractiveness of maize volatiles induced by Helicoverpa armigera and Pseudaletia separata to the generalist parasitoid Campoletis chlorideae. Entomol Exp Appl 118:87–96. https://doi.org/10.1111/j.1570-7458.2006.00368.x
Acknowledgements
We thank A. Prado (USP-ESALQ) for technical assistance.
Funding
This study was supported by the National Institute of Science and Technology (INCT) Semiochemicals in Agriculture (Conselho Nacional de Desenvolvimento Científico e Tecnológico-CNPq Process 573761/2008-6 and Fundação de Amparo à Pesquisa do Estado de São Paulo-FAPESP Process 2008/57701-2). NNG was funded by Estudantes-Convênio de Pós-Graduação (PEC-PG) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by: Sven Thatje
Electronic supplementary material
Online Resource 1
(DOCX 93 kb)
Rights and permissions
About this article
Cite this article
Naranjo-Guevara, N., Peñaflor, M.F.G.V., Cabezas-Guerrero, M.F. et al. Nocturnal herbivore-induced plant volatiles attract the generalist predatory earwig Doru luteipes Scudder. Sci Nat 104, 77 (2017). https://doi.org/10.1007/s00114-017-1498-9
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00114-017-1498-9