The Response of Susceptible and Pyrethroid-Resistant Blattella germanica (Dyctioptera: Blattellidae) to Shelter-Associated Cues.
Attractant
Faeces
German cockroach
Repellent
Resistant strains
Shelter
Journal
Neotropical entomology
ISSN: 1678-8052
Titre abrégé: Neotrop Entomol
Pays: Netherlands
ID NLM: 101189728
Informations de publication
Date de publication:
Oct 2023
Oct 2023
Historique:
received:
02
01
2023
accepted:
11
07
2023
pubmed:
8
8
2023
medline:
8
8
2023
entrez:
8
8
2023
Statut:
ppublish
Résumé
In this work, it was studied the role of faeces in the location and permanence in a shelter in susceptible and pyrethroid-resistant individuals of Blattella germanica (Linnaeus 1767). Additionally, the effect of different concentrations of palmitic acid on the modulation of these behaviours was tested. A shelter constituted by a square cardboard structure was offered to susceptible as well as to resistant specimens. The shelter bases were treated with faecal extracts obtained from susceptible or resistant cockroaches, or with solutions of palmitic acid. The behaviour of susceptible as well as resistant specimens was analysed using infrared videography software. Susceptible's faecal extract attracted both specimens since the time spent by cockroaches to locate the treated shelters was lower, whereas the faecal extract from resistant insects did not elicit any effect on both strains. Faecal extracts showed an arrestant effect on both strains, suggested by the time spent inside the shelter that was significantly higher in their presence. On the other hand, treatment with palmitic acid produced an attractant or a repellent effect depending on the concentration and strain. The tested lower concentration was attractant to susceptible insects, but did not produce any effect on resistant ones. In addition, the higher concentrations did not produce any effect on susceptible individuals, but resulted repellent for resistant ones. Palmitic acid did not produce an arrestant effect on the strains as there was not an increase in time spent inside the shelter in the presence of this substance. An increase in the number of visits to the shelter and to the periphery was also observed in shelters treated with the faecal extract and with the lower concentration of palmitic acid. These results show that compounds of the susceptible faeces were attractant to cockroaches of both strains, while faecal extracts from resistant insects were not. Moreover, a dual effect of palmitic acid was observed, being attractant at low concentrations and repellent as concentration increased. Additionally, a difference in the concentration threshold at which the effect of this substance changes was observed between strains.
Identifiants
pubmed: 37552458
doi: 10.1007/s13744-023-01071-z
pii: 10.1007/s13744-023-01071-z
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
848-859Informations de copyright
© 2023. Sociedade Entomológica do Brasil.
Références
Abbott KC, Dwyer G (2007) Food limitation and insect outbreaks: complex dynamics in plant-herbivore models. J Anim Ecol 76(5):1004–1014. https://doi.org/10.1111/j.1365-2656.2007.01263.x
doi: 10.1111/j.1365-2656.2007.01263.x
pubmed: 17714279
Alzogaray RA, Sfara V, Moretti AN, Zerba EN (2012) Behavioural and toxicological responses of Blattella germanica (Dictyoptera: Blattellidae) to monoterpenes. Eur J Entomol 110:247–252
doi: 10.14411/eje.2013.037
Ame JM, Rivault C, Deneubourg JL (2004) Cockroach aggregation based on strain odour recognition. Anim Behav 68:793–801
doi: 10.1016/j.anbehav.2004.01.009
Barrozo RB, Lazzari CR (2006) Orientation response of haematophagous bugs to CO2: the effect of the temporal structure of the stimulus. J Comp Physiol A 192:827–831
doi: 10.1007/s00359-006-0120-y
Berthold R, Wilson BR (1967) Resting behavior of the German cockroach, Blattella germanica. Ann Entomol Soc Am 60:347–351
doi: 10.1093/aesa/60.2.347
Bodin A, Vinauger C, Lazzari CR (2009) Behavioural and physiological state dependency of host seeking in the blood-sucking insect Rhodnius prolixus. J Exp Biol 212:2386–2393
pubmed: 19617431
doi: 10.1242/jeb.030668
Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White JSS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135
pubmed: 19185386
doi: 10.1016/j.tree.2008.10.008
Boné E, Aráoz B, González-Audino P, Sfara V (2022a) Feeding behaviour of a pyrethroid-resistant strain of the German cockroach Blattella germanica (Linnaeus, 1767). Neotrop Entomol 51:221–229. https://doi.org/10.1007/s13744-021-00937-4
Boné E, Acevedo GR, Sterkel M, Ons S, González-Audino P, Sfara V (2022b) Characterization of the pyrethroid resistance mechanisms in a Blattella germanica (Dictyoptera: Blattellidae) strain from Buenos Aires (Argentina). Bull Entomol Res 112:21–28
pubmed: 34229770
doi: 10.1017/S000748532100050X
Cochran DG (1989) Monitoring of insecticide resistance in field-collected strains of German cockroach. J Econ Entomol 82:336–341
pubmed: 2708624
doi: 10.1093/jee/82.2.336
Cornwell PB (1968) The cockroach. In: Volume 1. A laboratory insect and an industrial pest. The cockroach. Hutchinson, London
Denzer DJ, Fuchs MEA, Stein G (1988) ZumVerhalten von Blattella germanica L.: Aktionsradius und Refugientreue 1. J Appl Entomol 105:330–343
doi: 10.1111/j.1439-0418.1988.tb00195.x
Dicke M, Sabelis MW (1988) Infochemical terminology: based on cost-benefit analysis rather than origin of compounds? Funct Ecol 131–139
Di Rienzo J, Casanoves F, Balzarini M, Gonzalez L, Tablada M, Robledo YC (2011) InfoStat versión 2011. http://www.infostat.com.ar
Ebeling W, Reierson DA, Wagner RE (1967) Influence of repellency on the efficacy of blatticides. II. Laboratory experiments with German cockroaches. J Econ Entomol 60:1375–1390
pubmed: 6054445
doi: 10.1093/jee/60.5.1375
Faucher C, Forstreuter M, Hilker M, Bruyne M (2006) Behavioral responses of Drosophila to biogenic levels of carbon dioxide depend on life-stage, sex and olfactory context. J Exp Biol 209:2739–2748
pubmed: 16809465
doi: 10.1242/jeb.02297
Ferrero AA, Chopa CS, González JW, Alzogaray RA (2007) Repellence and toxicity of Schinus molle extracts on Blattella germanica. Fitoterapia 78:311–314
pubmed: 17490831
doi: 10.1016/j.fitote.2006.11.021
Fleischer J, Pregitzer P, Breer H, Krieger J (2018) Access to the odor world: olfactory receptors and their role for signal transduction in insects. Cell Mol Life Sci 75:485–508
pubmed: 28828501
doi: 10.1007/s00018-017-2627-5
Fontan A, Audino PG, Martinez A, Alzogaray RA, Zerba EN, Camps F, Cork A (2002) Attractant volatiles released by female and male Triatoma infestans (Hemiptera: Reduviidae), a vector of Chagas disease: chemical analysis and behavioral bioassay. J Med Entomol 39:191–197
pubmed: 11931256
doi: 10.1603/0022-2585-39.1.191
Foster SP, Tomiczek M, Thompson R, Denholm I, Poppy G, Kraaijeveld AR, Powell W (2007) Behavioural side-effects of insecticide resistance in aphids increase their vulnerability to parasitoid attack. Anim Behav 74:621–632
doi: 10.1016/j.anbehav.2006.12.018
Foster SP, Denholm I, Thompson R (2003) Variation in response to neonicotinoid insecticides in peach-potato aphids, Myzus persicae (Hemiptera: Aphididae). Pest Manag Sci Pest Sci 59:166–173
doi: 10.1002/ps.570
Fuchs VM, Franke S, Francke W (1985) Carbonsäuren im Kot von Blattella germanica (L.) und ihre mögliche Rolle als Teil des Aggregations pheromons. Z Angew Entomol 99:499–503
doi: 10.1111/j.1439-0418.1985.tb02017.x
Gemeno C, Williams GM, Schal C (2011) Effect of shelter on reproduction, growth and longevity of the German cockroach, Blattella germanica (Dictyoptera: Blattellidae). Eur J Entomol 108:205
doi: 10.14411/eje.2011.028
Grandcolas P (1998) Domestic and non-domestic cockroaches: facts versus received ideas. Rev Fr Allergol 38:833–838
Hamilton JA, Wada-Katsumata A, Schal C (2019) Role of cuticular hydrocarbons in German cockroach (Blattodea: Ectobiidae) aggregation behavior. Environ Entomol 48:546–553. https://doi.org/10.1093/ee/nvz044
doi: 10.1093/ee/nvz044
pubmed: 31034573
Haverkamp A, Hansson BS, Knaden M (2018) Combinatorial codes and labeled lines: how insects use olfactory cues to find and judge food, mates, and oviposition sites in complex environments. Front Physiol 9:49
pubmed: 29449815
pmcid: 5799900
doi: 10.3389/fphys.2018.00049
Heim JR, Weston DP, Major K, Poynton H, Hartz KEH, Lydy MJ (2018) Are there fitness costs of adaptive pyrethroid resistance in the amphipod, Hyalellaazteca? Environ Pollut 235:39–46
pubmed: 29274536
doi: 10.1016/j.envpol.2017.12.043
Ishii S (1970) An aggregation pheromone of the German cockroach, Blattella germanica (L.): 2. Species specificity of the pheromone. Appl Entomol Zool 5:33–41
doi: 10.1303/aez.5.33
Ishii S, Kuwahara Y (1968) Aggregation of German cockroach (Blattella germanica) nymphs. Experientia 24:88–89
pubmed: 5637632
doi: 10.1007/BF02136814
Ishii S, Kuwahara Y (1967) An aggregation pheromone of the German cockroach Blattella germanica L. (Orthoptera: Blattellidae): I. Site of the pheromone production. Appl Entomol Zool 2:203–217
doi: 10.1303/aez.2.203
Jeanson R, Rivault C, Deneubourg JL, Blanco S, Fournier R, Jost C, Theraulaz G (2005) Self-organized aggregation in cockroaches. Anim Behav 69:169–180
doi: 10.1016/j.anbehav.2004.02.009
Kakumanu ML, Maritz JM, Carlton JM, Schal C (2018) Overlapping community compositions of gut and fecal microbiomes in lab-reared and field-collected German cockroaches. Appl Environ Microbiol 84:01037–18
doi: 10.1128/AEM.01037-18
Keller JC, Clark PH, Lofgren CS (1956) Susceptibility of insecticide-resistant cockroaches to pyrethrins. I Pest Control 24(14–15):30
Kliot A, Ghanim M (2012) Fitness costs associated with insecticide resistance. Pest Manag Sci 68:1431–1437
pubmed: 22945853
doi: 10.1002/ps.3395
Kohler SL, Hoiland WK (2001) Population regulation in an aquatic insect: the role of disease. Ecology 82:2294–2305
doi: 10.1890/0012-9658(2001)082[2294:PRIAAI]2.0.CO;2
Lazzari CR (2009) Orientation towards hosts in haematophagous insects: an integrative perspective. Adv Insect Phys 37:1–58
doi: 10.1016/S0065-2806(09)37001-0
Ladonni H (2001) Evaluation of three methods for detecting permethrin resistance in adult and nymphal Blattella germanica (Dictyoptera: Blattellidae). J Econ Entomol 94:694–697
pubmed: 11425025
doi: 10.1603/0022-0493-94.3.694
Ledoux A (1945) Étude experimentale du grégarisme et de l’inter attraction sociale chez les Blattidés. Ann Sci Nat Zool Biol Anim 7:76–103
Lee HR, Kim GH, Choi WS, Park IK (2017) Repellent activity of Apiaceae plant essential oils and their constituents against adult German cockroaches. J Econ Entomol 110:552–557
pubmed: 28165121
doi: 10.1093/jee/tow290
Leppla NC, Koehler PG, Agee HR (1989) Circadian rhythms of the German cockroach (Dictyoptera: Blattellidae): locomotion in response to different photoperiods and wavelengths of light. J Insect Physiol 35:63–66
doi: 10.1016/0022-1910(89)90037-1
Loschiavo SR (1965) The chemosensory influence of some extracts of brewers’ yeast and cereal products on the feeding behavior of the confused flour beetle, Tribolium confusum (Coleoptera: Tenebrionidae). Ann Entomol Soc Am 58:576–588
doi: 10.1093/aesa/58.4.576
May-Concha I, Remón C, Mougabure-Cueto G (2020) Behavioral response mediated by feces in Triatoma infestans (Hemiptera: Reduviidae: triatominae) susceptible and resistant to deltamethrin. Acta Trop 206:105442
pubmed: 32171756
doi: 10.1016/j.actatropica.2020.105442
Metzger VR, Trier KH (1975) ZurBedeutung der Aggregations-Pheromone von Blattella germanica und Blatta orientalis. Angew Parasitol 1:16–27
Metzger R (1995) Behavior. In: Rust M, Owens J, Reierson D (eds) Understandingand controlling the German cockroach. Oxford University Press, Oxford, p 430
McFarlane JE, Alli I (1986) Aggregation of larvae of Blattella germanica (L.) by lactic acid present in excreta. J Chem Ecol 12:1369–1375
pubmed: 24307116
doi: 10.1007/BF01012356
Miller RG (1966) Simultaneous statistical inference. Springer, ISBN, p 9781461381228
Miller PF, Peters BA, Smith G (1996) Performance of Triflumuron against Blattella germanica (L). In: Proceedings of the second international conference on insect pests in the urban environment. Wheatons, Exeter, pp 145–146
Mori K, Fukamatsu K (1993) Synthesis of blattellastanoside A, a steroid glucoside isolated as the aggregation pheromone of the German cockroach. Proc Jpn Acad 69B:61–64
doi: 10.2183/pjab.69.61
Mori K, Fukamatsu K, Kido M (1993) Synthesis of chlorinated steroids related to the structures proposed for blattellastanosides A and B, the aggregation pheromone of the German cockroach Blattella Germanica L. l Liebigs Ann Chem 1993:657–663
doi: 10.1002/jlac.1993199301107
Navarro A, Utzet F, Puig P, Caminal J, Martin M (2001) Negative binomial distribution versus Poisson in the analysis of recurrent phenomena. Gac Sanit 15:447–452
pubmed: 11734158
doi: 10.1016/S0213-9111(01)71599-3
Pannunzi M, Nowotny T (2019) Odor stimuli: not just chemical identity. Front Physiol 10:1428
pubmed: 31827441
pmcid: 6890726
doi: 10.3389/fphys.2019.01428
Rehn JAG (1945) Man’s uninvited fellow-traveller—the cockroach. Sci Month 61:265–276
Ritter FJ, Persoons CJ (1975) Recent development in insect pheromone research, in particular in the Netherlands. Neth J Zool 25:261–275
doi: 10.1163/002829675X00281
Rivault C, Cloarec A, Sreng L (1998) Cuticular extracts inducing aggregation in the German cockroach, Blattella germanica (L.). J Insect Physiol 44:909–918
pubmed: 12770427
doi: 10.1016/S0022-1910(98)00062-6
Rivault C (1990) Distribution dynamics of Blattella germanica a closed urban environment. Entomol Exp App 57:85–91
doi: 10.1111/j.1570-7458.1990.tb01418.x
Rivault C (1989) Spatial distribution of the cockroach, Blattella germanica, in a swimming-bath facility. Entomol Exp App 53:247–255
doi: 10.1111/j.1570-7458.1989.tb03572.x
Rivero A, Magaud A, Nicot A, Vézilier J (2011) Energetic cost of insecticide resistance in Culex pipiens mosquitoes. J Med Entomol 48:694–700
pubmed: 21661333
doi: 10.1603/ME10121
Rostant WG, Bowyer J, Coupland J, Facey J, Hosken DJ, Wedell N (2017) Pleiotropic effects of DDT resistance on male size and behaviour. Behav Genetics 47:449–458
doi: 10.1007/s10519-017-9850-6
Roth LM, Willis ER (1960) The biotic associations of cockroaches. The Lord Baltimore Press, Baltimore
Rust MK, Owens JM, Reierson DA (eds) (1995) Understanding and controlling the German cockroach. Oxford University Press, New York, USA
Rust MK, Appel AG (1985) Intra-and interspecific aggregation in some nymphal blattellidae cockroaches (Dictyoptera: Blattellidae). Ann Entomol Soc Am 78:107–110
doi: 10.1093/aesa/78.1.107
Sakuma M, Fukimi H (1993) Aggregation arrestant pheromone of the German cockroach, Blattella germanica (L.) (Dictyoptera: Blattellidae): isolation and structure elucidation of blattellastanoside-A and -B. J Chem Ecol 1(19):2521–2541
doi: 10.1007/BF00980688
Sakuma M, Fukimi H (1991) Aggregation pheromone of the German cockroach, Blattella germanica (L.) (Dictyoptera: Blattellidae): Choice-chamber assay for arrestant component(s). Appl Entomol Zool 26:223–235
doi: 10.1303/aez.26.223
Sakuma M, Fukimi H (1990) The aggregation pheromone of the German cockroach, Blattella germanica (L.) (Dictyoptera: Blattellidae): isolation and identification of the attractant components of the pheromone. Appl Entomol Zool 25:355–368
doi: 10.1303/aez.25.355
Scherkenbeck J, Nentwig G, Justus K, Lenz J, Gondol D, Wendler G, Graef C (1999) Aggregation agents in German cockroach Blattella germanica: examination of efficacy. J Chem Ecol 25:1105–1119
doi: 10.1023/A:1020885926578
Semmelhack JL, Wang JW (2009) Select Drosophila glomeruli mediate innate olfactory attraction and aversion. Nature 459:218–223. https://doi.org/10.1038/nature07983
doi: 10.1038/nature07983
pubmed: 19396157
pmcid: 2702439
Sommer SH (1975) Aggregation behavior of Blattela germanica. Angew Parasitol 16:135
pubmed: 1190549
Tang Q, Bourguignon T, Willenmse L, De Coninck E, Evans T (2019) Global spread of the German cockroach, Blattella Germanica. Biol Invasions 21:693–707
doi: 10.1007/s10530-018-1865-2
Tsuji H (1966) Attractive and feeding stimulative effect of some fatty acids and related compounds on three species of cockroaches. Appl Entomol Zool 17:89–97
Verschut TA, Carlsson MA, Hambäck PA (2019) Scaling the interactive effects of attractive and repellent odours for insect search behaviour. Sci Rep 9:1–8
doi: 10.1038/s41598-019-51834-1
Vulinec K (1990) Collective security: aggregation by insects as a defense. In: Evans DL, Schmidt JO (eds) Insect Defenses: Adaptive Mechanisms and Strategies of Prey and Predators. State University of New York Press, New York, pp 251– 288
Wada-Katsumata A, Zurek L, Nalyanya G, Roelofs WL, Zhang A, Schal C (2015) Gut bacteria mediate aggregation in the German cockroach. Proc Natl Acad Sci USA 112:15678–15683
pubmed: 26644557
pmcid: 4697420
doi: 10.1073/pnas.1504031112
Wang C, Scharf ME, Bennett GW (2004) Behavioral and physiological resistance of the German cockroach to gel baits (Blattodea: Blattellidae). J Econ Entomol 97:2067–2072
pubmed: 15666766
doi: 10.1093/jee/97.6.2067
Wertheim B, van Baalen EJA, Dicke M, Vet LE (2005) Pheromone-mediated aggregation in nonsocial arthropods: an evolutionary ecological perspective. Annu Rev Entomol 50:321–346
pubmed: 15355243
doi: 10.1146/annurev.ento.49.061802.123329
Wertheim B, Marchais J, Vet LEM, Dicke M (2002) Allee effect in larval resource exploitation in Drosophila: an interaction among density of adults, larvae, and micro-organisms. Ecol Entomol 27:608–617
doi: 10.1046/j.1365-2311.2002.00449.x
White TCR (2008) The role of food, weather and climate in limiting the abundance of animals. Biol Rev 83:227–248
pubmed: 18557977
doi: 10.1111/j.1469-185X.2008.00041.x
Wileyto EP, Boush GM, Gawin LM (1984) Function of cockroach (Orthoptera: Blattidae) aggregation behavior. Environ Entomol 13:1557–1560
doi: 10.1093/ee/13.6.1557
Wileyto PE, Boush MG (1983) Attraction of the German cockroach, Blattella germanica (Orthoptera: Blatellidae), to some volatile food components. J Econ Entomol 76(4):752–756
doi: 10.1093/jee/76.4.752
Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R, vol 574. Springer, New York
doi: 10.1007/978-0-387-87458-6