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Reproductive interference between two serious pests, oriental fruit flies Bactrocera carambolae and B. dorsalis (Diptera: Tephritidae), with very wide but partially overlapping host ranges

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Abstract

Bactrocera carambolae and B. dorsalis (Diptera: Tephritidae) are extremely destructive pests of fruits and vegetables in the Asia-Pacific region. Earlier reports have described that B. carambolae and B. dorsalis, respectively, use mainly star fruit and mango, suggesting a certain level of host partitioning which can be ascribed neither to differences in larval food qualities nor host-specific parasitoid mortality. This study specifically examined reproductive interference (antagonistic sexual interaction) between B. carambolae and B. dorsalis as a potential factor strongly affecting their host partitioning. We observed mating behaviors, especially interspecific courtships and mating, by cohabiting the conspecific and heterospecific pairs together. Consequently, we quantified their effects on the reproductive success of females. Males of both species frequently courted their own females, but they also courted females of other species. Courtship refusal by females was not selective in males of either species. This incomplete discrimination of both sexes led to frequent occurrences of interspecific sexual interactions in both species, but only B. carambolae females showed reduced reproductive success. These results suggest that B. dorsalis, superior in reproductive interference, can occupy high-quality mango, whereas B. carambolae, inferior in reproductive interference, must use low-quality star fruit.

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References

  • Allwood AJ, Chinajariyawong A, Kristsaneepaiboon S, Drew RAI, Hamacek EL, Hancock DL, Hengsawad C, Jinpanin JC, Jirasurat M, Kong Krong C, Leong CTS, Vijaysegaran S (1999) Host plant records for fruit flies (Diptera: Tephritidae) in Southeast Asia. Raffles Bull Zool Suppl 7:1–92

    Google Scholar 

  • Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Soft 67:1–48

    Article  Google Scholar 

  • Bauer S, Samietz J, Berger U (2004) Sexual harassment in heterogeneous landscapes can mediate population regulation in a grasshopper. Behav Ecol 16:239–246

    Article  Google Scholar 

  • Bernays E, Graham M (1988) On the evolution of host specificity in phytophagous arthropods. Ecology 69:886–892

    Article  Google Scholar 

  • Broström G (2017) glmmML: generalized Linear Models with Clustering. R package ver. 1.0.2. https://CRAN.R-project.org/package=glmmML. Accessed 30 Mar 2018

  • Clarke AR, Allwood A, Chinajariyawong A, Drew RAI, Hengsawad C, Jirasurat M, Kong Krong C, Kritsaneepaiboon S, Vijaysegaran S (2001) Seasonal abundance and host use patterns of seven Bactrocera Macquart species (Diptera: Tephritidae) in Thailand and Peninsular Malaysia. Raffles Bull Zool 49:207–220

    Google Scholar 

  • Drew RAI, Romig MC (1997) Overview—Tephritidae in the Pacific and Southeast Asia. In: Allwood AJ, Drew RAI (eds) Management of Fruit Flies in the Pacific. ACIAR, Bruce ACT, pp 46–53

    Google Scholar 

  • Ehrlich PR, Raven H (1964) Butterflies and plants: a study of coevolution. Evolution 18:586–608

    Article  Google Scholar 

  • Fletcher BS (1987) The biology of Dacine fruit flies. Ann Rev Entomol 32:115–144

    Article  Google Scholar 

  • Friberg M, Leimar O, Wiklund C (2013) Heterospecific courtship, minority effects and niche separation between cryptic butterfly species. J Evol Biol 26:971–979

    Article  CAS  Google Scholar 

  • Fujii N, Sujiono Kago H, Hidaka N, Takakura KI, Honma A, Tsukada M, Sawada H, Nishida T (2016) A comparison of host utilization between sibling fruit flies Bactrocera carambolae and B. papayae (Diptera: Tephritidae) in west Java, Indonesia, serious quarantine pests of fruit. Jpn J Environ Entomol Zool 26:133–141 (in Japanese with English summary)

    Google Scholar 

  • Futuyma DJ, Agrawal AA (2009) Macroevolution and the biological diversity of plants and herbivores. Proc Natl Acad Sci USA 106:18054–18061

    Article  CAS  Google Scholar 

  • Gröning J, Hochkirch A (2008) Reproductive interference between animal species. Quart Rev Biol 83:257–282

    Article  Google Scholar 

  • Hibino Y, Iwahashi O (1989) Mating receptivity of wild type females for wild type males and mass-reared males in the melon fly, Dacus cucurbitae Coquillett (Diptera: Tephritidae). Appl Entomol Zool 24:152–154

    Article  Google Scholar 

  • Honma A, Kishi S, Noriyuki S, Kyogoku D (2012) The role of adaptive interspecific promiscuity in the history of ecological research. Jpn J Ecol 62:217–224 (in Japanese)

    Google Scholar 

  • Iwahashi O, Itô Y, Shiyomi M (1983) A field evaluation of the sexual competitiveness of sterile melon flies. Dacus (Zeugodacus) cucurbitae. Ecol Entomol 8:43–48

    Article  Google Scholar 

  • Iwaizumi R (2004) Species and host record of the Bactrocera dorsalis complex (Diptera: Tephritidae) detected by the plant quarantine of Japan. Appl Entomol Zool 39:327–333

    Article  Google Scholar 

  • Jefferies MJ, Lawton JH (1984) Enemy free space and the structure of ecological communities. Biol J Lin Soc 23:269–286

    Article  Google Scholar 

  • Kago H, Sawada H, Agus S, Takakura KI, Nishida T, Tsukada M (2012) A simple criterion for distinguishing between sympatric fruit flies Bactrocera carambolae and B. papayae (Diptera: Tephritidae) notorious pests of diverse fruits on Java. Jpn J Environ Entomol Zool 23:143–149

    Google Scholar 

  • Kaplan I, Denno RF (2007) Interspecific interactions in phytophagous insects revisited: a quantitative assessment of competition theory. Ecol Lett 10:977–994

    Article  Google Scholar 

  • Keese MC (1997) Does escape to enemy-free space explain host specialization in two closely related leaf-feeding beetles (Coleoptera: Chrysomelidae)? Oecologia 112:81–86

    Article  Google Scholar 

  • Kishi S, Nakazawa T (2013) Analysis of species coexistence co-mediated by resource competition and reproductive interference. Popul Ecol 55:305–313

    Article  Google Scholar 

  • Kishi S, Tsubaki Y (2014) Avoidance of reproductive interference causes resource partitioning in bean beetle females. Popul Ecol 56:73–80

    Article  Google Scholar 

  • Kishi S, Nishida T, Tsubaki Y (2009) Reproductive interference determines persistence and exclusion in species interactions. J Anim Ecol 78:1043–1049

    Article  Google Scholar 

  • Kuno E (1992) Competitive exclusion through reproductive interference. Res Popul Ecol 34:275–284

    Article  Google Scholar 

  • Kyogoku D, Nishida T (2013) The mechanism of the fecundity reduction in Callosobruchus maculatus caused by Callosobruchus chinensis males. Popul Ecol 55:87–93

    Article  Google Scholar 

  • Kyogoku D, Sota T (2017) A generalized population dynamics model for reproductive interference with absolute density dependence. Sci Rep 7:1996

    Article  Google Scholar 

  • McInnis DO, Rendon P, Jang E, van Sauers-Muller A, Sugayama R, Malavasi A (1999) Interspecific mating of introduced, sterile Bactrocera dorsalis with wild B. carambolae (Diptera: Tephritidae) in Suriname: a potential case for cross-species sterile insect technique. Ann Entomol Soc Am 92:758–765

    Article  Google Scholar 

  • McLain DK, Pratt AE (1999) The cost of sexual coercion and heterospecific sexual harassment on the fecundity of a host-specific, seed-eating insect (Neacoryphus bicrucis). Behav Ecol Sociobiol 46:164–170

    Article  Google Scholar 

  • Nishida R, Tan KH, Fukami H (1988) Cis-3,4-dimethoxy n-n amyl alcohol from the rectal glands of male Oriental fruit fly, Dacus dorsalis. Chem Exp 3:207–210

    CAS  Google Scholar 

  • Nishida T, Takakura KI, Iwao K (2015) Host specialization by reproductive interference between closely related herbivorous insects. Popul Ecol 57:273–281

    Article  Google Scholar 

  • Noriyuki S, Osawa N, Nishida T (2012) Asymmetric reproductive interference between specialist and generalist predatory ladybirds. J Anim Ecol 81:1077–1085

    Article  Google Scholar 

  • Ohsaki N, Sato Y (1994) Food plant choice of Pieris butterflies as a trade-off between parasitoid avoidance and quality of plants. Ecology 75:59–68

    Article  Google Scholar 

  • R Development Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.r-project.org/. Accessed 25 Jul 2017

  • Ribeiro JMC, Spielman A (1986) The Satyr Effect: a model predicting parapatry and species extinction. Am Nat 128:513–528

    Article  Google Scholar 

  • Schutze MK, Jessup A, Ul-Haq I, Vreysen MJB, Wornoayporn V, Vera MT, Clarke AR (2013) Mating compatibility among four pest members of the Bactrocera dorsalis fruit fly species complex (Diptera: Tephritidae). J Econ Entomol 106:695–707

    Article  CAS  Google Scholar 

  • Schutze MK, Aketarawong N, Amornsak W, Armstrong KF, Augustinos AA, Barr N, Bo W, Bourtzis K, Boykin LM, Caceres C, Cameron SL, Chapman TA, Chinvinijkul S, Chomic A, Meyer M, Drosopoulou E, Englezou A, Ekesi S, Gariou-Papalexiou A, Geib SM, Hailstones D, Hasanuzzaman M, Haymer D, Hee AKW, Hendrichs J, Jessup A, Ji Q, Khamis FM, Krosch MN, Leblanc L, Mahmood K, Malacrida AR, Mavracani-Tsipidou P, Mwatawala M, Nishida R, Ono H, Reyes J, Rubinoff D, Jose MS, Shelly TE, Srikachar S, Tan KH, Thanaphum S, Haq I, Vijaysegaran S, Wee SL, Yesmin F, Zacharopoulou A, Clarke AR (2014) Synonymization of key pest species within the Bactrocera dorsalis species complex (Diptera: Tephritidae): taxonomic changes based on a review of 20 years of integrative morphological, molecular, cytogenetic, behavioural and chemoecological data. Syst Entomol 40:456–471

    Article  Google Scholar 

  • Strong DR, Lawton JH, Southwood R (1984) Insects on plants: community patterns and mechanisms. Harvard University Press, Massachusetts

    Google Scholar 

  • Sugimoto A (1978) Egg collection method in mass rearing of the melon fly, Dacus cucurbitae Coquillett (Diptera: Tephritidae). Jpn J Appl Entomol Zool 22:60–67 (in Japanese with English summary)

    Article  Google Scholar 

  • Sun DB, Li J, Liu YQ, Crowder DW, Liu SS (2014) Effects of reproductive interference on the competitive displacement between two invasive whiteflies. Bull Entomol Res 104:334–346

    Article  Google Scholar 

  • Takahashi Y, Watanabe M (2010) Female reproductive success is affected by selective male harassment in the damselfly Ischnura senegalensis. Anim Behav 79:211–216

    Article  Google Scholar 

  • Tan KH, Nishida R (1996) Sex pheromone and mating competition after methyl eugenol consumption in the Bactrocera dorsalis complex. In: McPheron BA, Steck GJ (eds) Fruit fly pests: a world assessment of their biology and management. CRC Press, Florida, pp 147–153

    Google Scholar 

  • Thompson JN (1988) Evolutionary ecology of the relationship between oviposition preference and performance of offspring in phytophagous insects. Entomol Exp Appl 47:3–14

    Article  Google Scholar 

  • Wee SL (2000) Behavior and reproductive ecology of Bactrocera carambolae and B. papayae. PhD thesis. Universiti Sains Malaysia, Penang

  • Wee SL, Tan KH (2000a) Interspecific mating of two sibling species of the Bactrocera dorsalis complex in a field cage. In: Tan KH (ed) Area-wide control of fruit flies and other pest insects. Universiti Sains Malaysia, Penang, pp 667–674

    Google Scholar 

  • Wee SL, Tan KH (2000b) Sexual maturity and intraspecific mating success of two sibling species of the Bactrocera dorsalis complex. Entomol Exp Appl 94:133–139

    Article  Google Scholar 

  • Wee SL, Tan KH (2005) Evidence of natural hybridization between two sympatric sibling species of Bactrocera dorsalis complex based on pheromone analysis. J Chem Ecol 31:845–858

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Mr. Ruswandi and Mr. Suburoto, Director and Former Director of the Pest Forecasting Center (BBPOPT), Ministry of Agriculture Indonesia, for providing laboratory facilities and laboratory-reared insects. We also thank Mr. Firdaus, Mr. Surono and Mr. Imroni of BBPOPT, for preparation and supporting of our study. Autolyzed yeast, a main ingredient of the food for adult fruit flies, was supplied by Asahi Food and Health Care Co., Ltd., Tokyo, Japan. This study was supported by JSPS KAKENHI Grant numbers 22405019 and 25304048.

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Authors and Affiliations

  1. Graduate School of Environmental Science, The University of Shiga Prefecture, 2500 Hassaka, Hikone, Shiga, 522-8533, Japan

    Daisuque Kitano, Nobuyuki Fujii, Shigemasa Yamaue, Atsushi Honma, Takayoshi Nishida, Hiroichi Sawada & Koh-Ichi Takakura

  2. Balai Besar Peramalan Organisme Pengganggu Tumbuhan, Jl. Raya Kaliasin Tromol Pos 1, Jatisari, Karawang, 41374, West Java, Indonesia

    Sujiono

  3. Graduate School of Bioresources, Mie University, Tsu, Mie, 514-8507, Japan

    Tasuku Kitamura & Morio Tsukada

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  1. Daisuque Kitano
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  2. Nobuyuki Fujii
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Correspondence to Daisuque Kitano.

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Kitano, D., Fujii, N., Sujiono et al. Reproductive interference between two serious pests, oriental fruit flies Bactrocera carambolae and B. dorsalis (Diptera: Tephritidae), with very wide but partially overlapping host ranges. Appl Entomol Zool 53, 525–533 (2018). https://doi.org/10.1007/s13355-018-0584-6

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