Abstract
Most people consider cockroaches to be quintessential urban pests, even though very few of the 5000 cockroach species live in urban areas. The German cockroach is the most widespread and common cockroach in urban areas, however how this invasive species has spread globally is poorly understood. We reviewed the published and grey literatures, and museum data, to document the spread of the German cockroach, and how it may have interacted with other urban cockroach species. We found that the German cockroach likely originated from South Asia, was introduced into Europe no later than the 18th century, from where it invaded worldwide. The spread of the German cockroach was facilitated by the improvement of transportation technologies, especially from colonial trading, and indoor heating in cooler climates. Studies of population genetics have found that once introduced into a new location, the German cockroach spread rapidly through local expansion, and this could be within single (large, multiple-story) buildings. This local expansion resulted in displacement of other urban cockroach species, likely due to their small size requiring fewer resources, shorter generation times and so faster evolution, especially for pesticide resistance. These findings may help to identify new pest management methods. Future research could use genetic tools at larger scales to map distribution routes across the globe and interaction with pesticides and the evolution of resistance.
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References
Appel AG, Smith LM (2002) Biology and management of the smokybrown cockroach. Annu Rev Entomol 47(1):33–55
Appel AG, Reierson DA, Rust MK (1983) Comparative water relations and temperature sensitivity of cockroaches. Comp Biochem Physiol, A: Comp Physiol 74(2):357–361
Appel AG, Eva MJ, Snoddy ET (2009) Distribution of the Asian cockroach, Blattella asahinai (Dictyoptera: Blattellidae), in Dothan, Alabama. J Ala Acad Sci 80(1):1–10
Ascunce MS, Yang CC, Oakey J, Calcaterra L, Wu WJ, Shih CJ, Goudet J, Ross KG, Shoemaker D (2011) Global invasion history of the fire ant Solenopsis invicta. Science 331(6020):1066–1068
Austin JW, Glenn GJ, Szalanski AL, McKern JA, Gold RE (2007) Confirmation of Asian cockroach Blatella asahinai (Blattodea: Blattelidae) introduction to Texas based on genetics, morphology, and behavior. Fla Entomol 90(3):574–576
Beier M (1974). Blattariae (Schaben). Handbuch der Zoologie, Arthropoda: Insecta. 2. Walter de Gruyter, Berlin, Germany. 1–127
Bell WJ, Adiyodi K (1982) The american cockroach. Springer, Dordrecht
Bell WJ, Roth LM, Nalepa CA (2007) Cockroaches: ecology, behavior, and natural history. JHU Press, Baltimore
Bohn H (1984) The nearest relative of the oriental cockroach (Blatta orientalis) (Insecta: Blattodea: Blattidae). Israel J Zool 33(1–2):39–50
Boissin E, Hurley B, Wingfield MJ, Vasaitis R, Stenlid J, Davis C, de Groot P, Ahumada R, Carnegie A, Goldarazena A, Klasmer P, Wermelinger B, Slippers B (2012) Retracing the routes of introduction of invasive species: the case of the Sirex noctilio woodwasp. Mol Ecol 21(23):5728–5744
Bolivar I (1884) Artropodos del Viaje al Pacifico verificado de 1862 a 1865 por una comision de naturalistas enviada por el Gobierno Espanol. Insectos Neuropteros y Ortopteros, pp.124
Booth W, Santangelo RG, Vargo EL, Mukha DV, Schal C (2010) Population genetic structure in German cockroaches (Blattella germanica): differentiated islands in an agricultural landscape. J Hered 102:175–183
Boursot P, Din W, Anand R, Darviche D, Dod BV, Von Deimling F, Talwar G, Bonhomme F (1996) Origin and radiation of the house mouse: mitochondrial DNA phylogeny. J Evol Biol 9(4):391–415
Boyer S, Rivault C (2003) La Réunion and Mayotte cockroaches: impact of altitude and human activity. CR Biol 326:210–216
Boyer S, Rivault C (2006) Impact of human activity on the distribution of native and non-native cockroach species (Dictyoptera) in La Réunion and Mayotte. B Entomol Res 96(04):399–406
Brunner von Wattenwyl KB (1865) Nouveau système des Blattaires. G. Braumüller, Vienne
Brünnich MT (1763) Den Danske Atlas eller Kongenget Dannemark In E. Pontoppidan, Copenhagen, Denmark
Burgess NRH, Chetwyn KN (1979) Cockroaches and the hospital environment. Nurs Times 75(7):suppl 5
Chamberlin JC (1949) Insects of agricultural and household importance in Alaska, with suggestions for their control. Alaska Agric Exp Stn 9:1–59
Chen T, Zhang Y (2007) Kangxizidian. Social Sciences Academic Press, Beijing
Cloarec A, Rivault C, Cariou M (1999) Genetic population structure of the German cockroach, Blattella germanica: absence of geographical variation. Entomol Exp Appl 92(3):311–319
Cochran DG (1999) Cockroaches: their biology, distribution and control. World Health Organization, Geneva
Copeland M (2003) Cockroach. Reaktion Books Ltd., London
Cornwell PB (1968) The cockroach, vol 1. Hutchinson, London, pp 1–366
Cornwell PB (1976) The cockroach. Volume II. Insecticides and cockroach control. The Rentokil Library, London
Crissman JR, Booth W, Santangelo RG, Mukha DV, Vargo EL, Schal C (2010) Population genetic structure of the German cockroach (Blattodea: Blattellidae) in apartment buildings. J Med Entomol 47(4):553–564
Cucchi T, Vigne JD, Auffray JC (2005) First occurrence of the house mouse (Mus musculus domesticus Schwarz & Schwarz, 1943) in the Western Mediterranean: a zooarchaeological revision of subfossil occurrences. Biol J Linn Soc 84(3):429–445
Curry A (1979) The insects associated with the Manchester mummies. The Manchester Museum Mummy Project, Manchester Museum, Manchester, Manchester, pp 113–118
Dambach M, Goehlen B (1999) Aggregation density and longevity correlate with humidity in first-instar nymphs of the cockroach (Blattella germanica L., Dictyoptera). J Insect Physiol 45(5):423–429
Danchin E, Giraldeau LA, Valone TJ, Wagner RH (2004) Public information: from nosy neighbors to cultural evolution. Science 305(5683):487–491
Darwin C (1859) On the origin of the species by natural selection. Murray, London
de Saussure H (1864) Orthoptères de l’Amérique moyenne. Impr. Ramboz et Schuchardt, Geneva
Duan Y (1815) Commentaries to the Shuowen jiezi
Durbin EJ, Cochran DG (1985) Food and water deprivation effects on reproduction in female Blattella germanica. Entomol Exp Appl 37(1):77–82
Durier V, Rivault C (2001) Effects of spatial knowledge and feeding experience on foraging choices in German cockroaches. Anim Behav 62(4):681–688
Ebeling W (1978) Urban entomology. Division of Agricultural Sciences. University of California, Davis
Ffrench-Constant RH, Anthony N, Aronstein K, Rocheleau T, Stilwell G (2000) Cyclodiene insecticide resistance: from molecular to population genetics. Annu Rev Entomol 45(1):449–466
Fitzpatrick BM, Fordyce JA, Niemiller ML, Reynolds RG (2011) What can DNA tell us about biological invasions? Biol Invasions 14(2):245–253
Flegr J (2013) Microevolutionary, macroevolutionary, ecological and taxonomical implications of punctuational theories of adaptive evolution. Biol Direct 8(1):1
Frankie GW, Ehler L (1978) Ecology of insects in urban environments. Annu Rev Entomol 23(1):367–387
Gadot M, Burns E, Schal C (1989) Juvenile hormone biosynthesis and oocyte development in adult female Blattella germanica: effects of grouping and mating. Arch Insect Biochem 11(3):189–200
Grandcolas P (1998) Domestic and non-domestic cockroaches: facts versus received ideas. Rev Fr Allergol 38(10):833–838
Guillemaud T, Ciosi M, Lombaert E, Estoup A (2011) Biological invasions in agricultural settings: insights from evolutionary biology and population genetics. CR Biol 334(3):237–246
Gunn DL (1935) The temperature and humidity relations of the cockroach. III. A comparison of temperature preference, and rates of desiccation and respiration of Periplaneta americana, Blatta orientalis and Blatella germanica. J Exp Biol 12(185):90
Heal RE, Nash R, Williams M (1953) An insecticide-resistant strain of the German Cockroach from Corpus Christi. Texas. J Econ Entomol 46(2):385–386
Hitomi M (1957) Cockroaches prevalentin oversea vessels with special reference to Blattella germanica L. Med Entomol Zool 8(3):112–118
Holbrook GL, Armstrong E, Bachmann JAS, Deasy BM, Schal C (2000) Role of feeding in the reproductive ‘group effect’ in females of the German cockroach Blattella germanica (L.). J Insect Physiol 46(6):941–949
Huang Y, Zhang WG (2010) Efficacy of baits to cockroach in the passenger liner. Chin J Hyg Insect Equip 2(10):118–120
Huldén L, Huldén L (2003) Den orientaliska och den tyska kackerlackans ankomst till Finland. Entomol tidskr 124(4):201–207
Hulme-Beaman A, Dobney K, Cucchi T, Searle JB (2016) An ecological and evolutionary framework for commensalism in anthropogenic environments. Trends Ecol Evol 31(8):633–645
Izutsu M, Ueda S, Ishii S (1970) Aggregation effects on the growth of the German cookroach, Blattella germanica (L.)(Blattaria: Blattellidae). Appl Entomol Zool 5(3):159–171
Jeanson R, Deneubourg JL (2006) Path selection in cockroaches. J Exp Biol 209(23):4768–4775
Jobet E, Durand P, Langand J, Muller-Graf CDM, Hugot JP, Bougnoux ME, Rivault C, Cloarec A, Morand S (2000) Comparative genetic diversity of parasites and their hosts: population structure of an urban cockroach and its haplo-diploid parasite (Oxyuroid nematode). Mol Ecol 9(4):481–486
Kark S, Iwaniuk A, Schalimtzek A, Banker E (2007) Living in the city: can anyone become an “urban exploiter”? J Biogeogr 34(4):638–651
Kramer R, Brenner R (2009) Cockroaches (Blattaria). In: Mullen GR, Durden LA (eds) Medical and veterinary entomology. Academic Press, Cambridge, pp 43–56
Kutrup B (2002) Cockroach infestation in some hospitals in Trabzon, Turkey. Turk J Zool 27(1):73–77
Labbe P, Lenormand T, Raymond M (2005) On the worldwide spread of an insecticide resistance gene: a role for local selection. J Evol Biol 18(6):1471–1484
Landau I, Müller G, Schmidt M (1999) The urban pest advisory service of Zurich (Switzerland) and the situation of some selected pests. In Proceedings of the Third International Conference on Urban Pests, Czech Republic: Grafické závody Hronov
Ligon R, True A (1673) Exact history of the island of Barbadoes. Self Published, London
Lihoreau M, Rivault C (2008) Tactile stimuli trigger group effects in cockroach aggregations. Anim Behav 75(6):1965–1972
Lihoreau M, Rivault C (2009) Kin recognition via cuticular hydrocarbons shapes cockroach social life. Behav Ecol 20(1):46–53
Lihoreau M, Rivault C (2010) German cockroach males maximize their inclusive fitness by avoiding mating with kin. Anim Behav 80(2):303–309
Lihoreau M, Zimmer C, Rivault C (2007) Kin recognition and incest avoidance in a group-living insect. Behav Ecol 18(5):880–887
Lihoreau M, Zimmer C, Rivault C (2008) Mutual mate choice: when it pays both sexes to avoid inbreeding. PLoS ONE 3(10):e3365
Lihoreau M, Brepson L, Rivault C (2009) The weight of the clan: even in insects, social isolation can induce a behavioural syndrome. Behav Process 82(1):81–84
Lihoreau M, Deneubourg JL, Rivault C (2010) Collective foraging decision in a gregarious insect. Behav Ecol Sociobiol 64(10):1577–1587
Lihoreau M, Costa JT, Rivault C (2012) The social biology of domiciliary cockroaches: colony structure, kin recognition and collective decisions. Insect Soc 59(4):445–452
Limoee M (2012) A review on insecticide resistance in German cockroach Blattella germanica (L.)(Dictyoptera: Blattellidae) from Iran. Healthmed 6(9):3101–3106
Linnaeus C (1758) Systema naturae, vol 1. Engelman, Leipzi
Linnaeus C (1767) Systema naturae, ed. 12, vol. 2. Salvii, Holmiae, Sweden
Liu N, Zhu F, Xu Q, Pridgeon JW, Gao X (2005) Behavioral change, physiological modification, and metabolic detoxification: mechanisms of insecticide resistance. Acta Entomol Sinica 49(4):671–679
Lombaert E, Guillemaud T, Lundgren J, Koch R, Facon B, Grez A, Loomans A, Malausa T, Nedved O, Rhule E, Staverlokk A, Steenberg T, Estoup A (2014) Complementarity of statistical treatments to reconstruct worldwide routes of invasion: the case of the Asian ladybird Harmonia axyridis. Mol Ecol 23(24):5979–5997
Mack RN, Simberloff D, Mark Lonsdale W, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10(3):689–710
Mallis A, Easterlin WC, Astor RJ (1986) Resistance in a large cockroach, Periplaneta brunnea, in Florida. Pest Control 34:22
Martin LJ, Adams RI, Bateman A et al (2015) Evolution of the indoor biome. Trends Ecol Evol 30(4):223–232
McIntyre NE (2000) Ecology of urban arthropods: a review and a call to action. Ann Entomol Soc Am 93(4):825–835
McKinney ML (2002) Urbanization, biodiversity, and conservation: the impacts of urbanization on native species are poorly studied, but educating a highly urbanized human population about these impacts can greatly improve species conservation in all ecosystems. Bioscience 52(10):883–890
Mellanby K (1939) Low temperature and insect activity. Proc R Soc Lond B Biol Sci 127:473–487
Miall LC (1886) The structure and life-history of the cockroach (Periplaneta orientalis): an introduction to the study of insects. L. Reeve & Company, London, p 224
Miller D, Koehler P (2000) Trail-following behavior in the German cockroach (Dictyoptera: Blattellidae). J Econ Entomol 93(4):1241–1246
Mizukubo T (1981) A revision of the genus Blattella (Blattaria: Blattellidae) of Japan. I. Terminology of the male genitalia and description of a new species from Okinawa Island. Esakia 17:149–159
Mukha D (2002) Wiegmann BM and Schal C, Evolution and phylogenetic information content of the ribosomal DNA repeat unit in the Blattodea (Insecta). Insect Biochem Molec 32(9):951–960
Mukha DV, Kagramanova AS, Lazebnaya IV, Lazebnyi OE, Vargo EL, Schal C (2007) Intraspecific variation and population structure of the German cockroach, Blattella germanica, revealed with RFLP analysis of the non-transcribed spacer region of ribosomal DNA. Med Vet Entomol 21(2):132–140
Mukha DV, Mysina V, Mavropulo V, Schal C (2010) Structure and molecular evolution of the ribosomal DNA external transcribed spacer in the cockroach genus Blattella. Genome 54(3):222–234
Naqqash MN, Gokce A, Bakhsh A, Salim M (2016) Insecticide resistance and its molecular basis in urban insect pests. Parasitol Res 115(4):1363–1373
Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29(1):1
Owens J, Bennett G (1982) German cockroach movement within and between urban apartments. J Econ Entomol 75(4):570–573
Parker PG, Snow AA, Schug MD, Booton GC, Fuerst PA (1998) What molecules can tell us about populations: choosing and using a molecular marker. Ecology 79(2):361
Pedigo LP, Rice ME (2014) Entomology and pest management. Waveland Press, Long Grove
Peterson M (1977) Reach for new world. Natl Geogr 152(6):724–767
Peterson RK, Shurdut BA (1999) Human health risks from cockroaches and cockroach management: a risk analysis approach. Am Entomol 45(3):142–148
Pfannenstiel RS, Booth W, Vargo EL, Schal C (2008) Blattella asahinai (Dictyoptera: Blattellidae): A new predator of lepidopteran eggs in South Texas soybean. Ann Entomol Soc Am 101(4):763–768
Princis K (1950) Entomological results from the Swedish expedition 1934 to Burma and British India. ArkZool 1:203–222
Princis K (1954) Wo ist die Urheimat von Blatta orientalis L. zu suchen? Opuscula Entomol 19:202–204
Princis K (1958) Revision of the Walker and Kirby types of Blattaria in British museum of Natural History, London II. Opusc Entomol 23:59–75
Princis K (1969) subordo Epilamproidea, Family Blattellidae. Orthopterorum Catalogus Pt 13:713–1020
Princis K, Beier M (1966) Pars 8: Blattariae: Blattoidea: Blattidae, Nocticolidae. Orthopterorum Catalogus. Junk, Gravenhage, pp 402–614
Pugh P (1994) Non-indigenous Acari of Antarctica and the sub-Antarctic islands. Zool J Linn Soc 110(3):207–217
Ragge DR (1965) Grasshoppers, crickets and cockroaches of the British Isles. Warne & Co., Ltd., London
Rasmussen A, Nielsen P (1997) Some of the cases and characteristic variations in number of inquiries in 1997. Danish Pest Information Laboratory Annual Report. pp.48-49
Rehn JA (1945) Man’s uninvited fellow traveler-the cockroach. Sci Month 61(4):265–276
Rivault C (1989) Spatial distribution of the cockroach, Blattella germanica, in a swimming-bath facility. Entomol Exp Appl 53(3):247–255
Rivault C, Cloarec A, Sreng L (1998) Cuticular extracts inducing aggregation in the German cockroach, Blattella germanica (L.). J Insect Physiol 44(10):909–918
Robinson W (1999) The changing status of the German cockroach in the urban environment. In: Proceedings of the New Zealand plant protection conference. pp 16–21
Robinson WH (2005) Urban insects and arachnids: a handbook of urban entomology. Cambridge University Press, Cambridge
Roth LM (1970) Interspecific mating in Blattaria. Ann Entomol Soc Am 63(5):1282–1285
Roth LM (1985) A taxonomic revision of the genus Blattella Caudell (Dictyoptera, Blattaria: Blattellidae). Entomol Scand Suppl 22:1–221
Roth LM (1986) Blattella asahinai introduced into Florida (Blattaria: Blattellidae). Psyche 93(3–4):371–374
Roth LM (1997) A new combination, and new records of species of Blattella Caudell (Blattaria: Blattellidae: Blattellinae). Orient Insects 31(1):229–239
Roth LM, Cohen S (1973) Aggregation in Blattaria. Ann Entomol Soc Am 66(6):1315–1323
Roth LM, Rivault C (2002) Cockroaches from some islands in the Indian Ocean: La Réunion, Comoro, and Seychelles (Dictyoptera: Blattaria). Trans Am Entomol Soc 128:43–74
Roth LM, Willis E (1960) The biotic associations of cockroaches, vol 141. Smithsonian Miscellaneous Collections, Washington
Rust MK, Owens JM, Reierson DA (1995) Understanding and controlling the German cockroach. Oxford University Press, Oxford
Schal C, Hamilton R (1990) Integrated suppression of synanthropic cockroaches. Annu Rev Entomol 35(1):521–551
Shahraki GH, Parhizkar S, Nejad ARS (2013) Cockroach infestation and factors affecting the estimation of cockroach population in urban communities. Int J Zool 2013:1–6
Shaw E (1925) New genera and species (mostly Australasian) of Blattidae, with notes and some remarks on Tepper’s types. In: Proceedings of The Linnean Society of New South Wales, pp 171–213
Sherk B (2004) 500 Years of New Words: the fascinating story of how, when, and why these words first entered the English language. Dundurn, Toronto
Shuckburgh ES (1888) The epistles of Horace. University Press, Cambridge
Snoddy ET, Appel AG (2008) Distribution of Blattella asahinai (Dictyoptera: Blattellidae) in Southern Alabama and Georgia. Ann Entomol Soc Am 101(2):397–401
Solomon M, Adamson BE (1955) The powers of survival of storage and domestic pests under winter conditions in Britain. B Entomol Res 46(2):311–355
Stejskal V, Verner P (1996) Long-term changes of cockroach infestations in Czech and Slovak food-processing plants. Med Vet Entomol 10(1):103–104
Tang Q, Jiang H, Li Y, Bourguignon T, Evans TA (2016) Population structure of the German cockroach, Blattella germanica. Biol Invasions 18(8):2391–2402
Topsell E (1658) The history of four-footed beasts and serpents. G. Sawbridge, T. Williams & T. Johnson, London, UK
Tsai CW, Lee HJ (2001) Analysis of specific adaptation to a domicile habitat: a comparative study of two closely related cockroach species. J Med Entomol 38(2):245–252
Vargo EL, Crissman JR, Booth W, Santangelo RG, Mukha DV, Schal C (2014) Hierarchical genetic analysis of German cockroach (Blattella germanica) populations from within buildings to across continents. PLoS ONE 9(7):e102321
Vidlička Ľ (2001) Fauna Slovenska Blattaria–šváby Mantodea–Modlivky (Insecta: Orthopteroidea). Veda, vydavateľstvo SAV, Bratislava
Vršanský P (2008) Mesozoic relative of the common synanthropic German cockroach (Blattodea). Dtsch Entomol Z 55(2):215–221
Vršanský P, Cifuentes-Ruiz P, Vidlička Ľ, Čiampor F, Vega F (2011) Afro-Asian cockroach from Chiapas amber and the lost Tertiary American entomofauna. Geol Carpath 62(5):463–475
Vršanský P, Oružinský R, Barna P, Vidlička L, Labandeira CC (2014) Native Ectobius (Blattaria: Ectobiidae) from the early Eocene Green River formation of Colorado and its reintroduction to North America 49 million years later. Ann Entomol Soc Am 107(1):28–36
Wang ZQ, Che YL, Feng PZ (2010) A taxonomic study of the genus Blattella Caudell, 1903 from China with description of one new species (Blattaria: Blattellidae). Acta Entomol Sin 53(8):908–913
Webb JE (1961) Resistance of some species of cockroaches to organic insecticides in Germany and France. J Econ Entomol 54(4):1956–1959
Weidner H (1983) Neue untersuchungen über vorkommen und verbreitung der schaben in der DDR und einige bemerkungen über die relative häufigkeitszunahme der Deutschen Schabe. Der prakt Schädlingsbek 35:151–153
Willis ER, Lewis N (1957) The longevity of starved cockroaches. J Econ Entomol 50:438–440
Wright S (1943) Isolation by distance. Genetics 28(2):114
Wu Z, Zhou T, Xiao P (1988) Xinhua Compendium of Materia Medica. Shanghai Science and Technology Publishing House, Shanghai
Zhu F, Lavine L, O’Neal S, Lavine M, Foss C, Walsh D (2016) Insecticide resistance and management strategies in urban ecosystems. Insects 7(1):2
Acknowledgements
This work was supported by NUS (National University of Singapore) Research Scholarship from Ministry of Education, Singapore and the Lee Hiok Kwee Endowed Fund of the Department of Biological Sciences, National University of Singapore, Singapore. TB thanks the Internal Grant Agency of the Faculty of Forestry and Wood Sciences, Czech University of Life Sciences (IGA A11/16), and was supported by a postdoctoral fellowship from the University of Sydney. We thank L. Vidlička for providing his translation of his work and ideas about the etymological history of cockroaches.
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Tang, Q., Bourguignon, T., Willenmse, L. et al. Global spread of the German cockroach, Blattella germanica. Biol Invasions 21, 693–707 (2019). https://doi.org/10.1007/s10530-018-1865-2
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DOI: https://doi.org/10.1007/s10530-018-1865-2