Skip to main content
SpringerLink
Log in

Globular galls on Haloxylon (Centrospermae: Chenopodiaceae) induced by gall midges, and the corresponding parasitoids in China

  • Original Research Paper
  • Published:
Applied Entomology and Zoology Aims and scope Submit manuscript

Abstract

The concealed gall inducers represent a significant challenge for both study and control within the realm of pest management. Gaining an understanding of the natural enemies that influence gall inducer populations is essential for the development of effective integrated pest control strategies. Haloxylon spp. are dominant xerophyte species that possess substantial ecological importance due to their roles in shelter provision and sand fixation. This study aimed to determine the main gall inducers that induce globular galls on both H. ammodendron and H. persicum and the parasitoid complex associated with them. Totally, two species of gall inducers and four species of parasitoids were obtained from the globular galls. Suaediola sp. was recorded as the predominant gall inducer, exhibiting biannual generational turnover. Both Torymus sp. and Mesopolobus quadrimaculatus were primary solitary koinobiont ectoparasitoids of gall midges, while only Platygaster sp. was endoparasitoid. Torymus sp. established dominance among the parasitoids, demonstrating a predilection for attacking first instar larvae. We also found that temperature variations significantly influenced the emergence and lifespan of the insects recorded from the galls, with a consistent trend of shortened wasp lifespan correlating with increasing temperature. According to these results, we conclude Torymus sp. could have an important potential to control gall inducers within closed galls and, therefore, should be considered for inclusion in the integrated pest management programs of Haloxylon forests in China.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

The data that support the findings of this study are available from the corresponding author, [H H-Y], upon reasonable request.

References

  • Arabzadeh N (2013) The impact of drought stress on photosynthetic quantum yield in Haloxylon aphyllum and Haloxylon persicum. Can Am Slav Stud 7:185–189

    CAS  Google Scholar 

  • Araújo WSD, Maia VC (2021) Topological structure of a tritrophic network composed of host plants, gall-inducing insects and parasitoids in a resting area in brazil. Entomol Sci 24:201–216

    Article  Google Scholar 

  • Baoer-han D, Zhang HF, Zhu YL, Zhang JL (2019) Spatial pattern and influence factors of natural regeneration of Haloxylon ammodendron seedlings in Zhungeer Basin. J West China for Sci 48:130–134

    Google Scholar 

  • Bari MN, Jahan M, Islam KS (2015) Effects of temperature on the life table parameters of Trichogramma zahiri (Hymenoptera: Trichogrammatidae), an egg parasitoid of Dicladispa armigera (Chrysomelidae: Coleoptera). Environ Entomol 44:368–378

    Article  CAS  PubMed  Google Scholar 

  • Bell RC, Belmaker A, Couch CS, Marchetto KM, Simonis JL, Thomas RQ, Sparks JP, Brown JM, Francisco KS, Manuel ME (2013) Effectiveness of Erythrina gall wasp biocontrol and implications for the recovery of threatened Wiliwili trees (Fabaceae: Erythrina sandwicensis). J Torrey Bot Soc 140:215–224

    Article  Google Scholar 

  • Buras A, Wucherer W, Zerbe S, Noviskiy Z, Muchitdinov N, Shimshikov B, Zverev N, Schmidt S, Wilmking M, Thevs N (2012) Allometric variability of Haloxylon species in central Asia. For Ecol Manage 274:1–9

    Article  Google Scholar 

  • Chen YS, Chen C, He HM, Xia QW, Xue FS (2013) Geographic variation in diapause induction and termination of the cotton bollworm, Helicoverpa armigera Hübner (Lepidoptera: Noctuidae). J Insect Physiol 59:855–862

    Article  CAS  PubMed  Google Scholar 

  • Chen PY, Feng HQ, Li GP, Niu YT, Qiu F, Qiang XJ (2015) Impacts of temperature and photophase on diapause termination of Adelphocoris suturalis. Plant Prot-CN 41:143–145

    CAS  Google Scholar 

  • Dang Hoa T, Khac P, Ueno T, Takagi M (2012) Effects of temperature and host on the immature development of the parasitoid Neochrysocharis okazakii (Hymenoptera: Eulophidae). J Fac Agr Kyushu U 57:133–137

    Google Scholar 

  • De YU, Jun Z, Mei WU, Wang G, Weng S, Shen J (2000) Biological characteristics of Aiolomorphus rhopaloides and Diomorus aiolomorphi. J Zhejiang A & F College 17:112–114

    Google Scholar 

  • Dittrich-Schroeder G, Harney M, Neser S, Joffe T, Bush S, Hurley BP, Wingfield MJ, Slippers B (2014) Biology and host preference of Selitrichodes neseri: a potential biological control agent of the Eucalyptus gall wasp, Leptocybe invasa. Biol Control 78:33–41

    Article  Google Scholar 

  • Dzhanokmen KA (2005) Review of species of the genus Mesopolobus Westwood (Hymenoptera, Chalcidoidea, Pteromalidae) from Kazakhstan. Tethys Entomol Res 11:71–80

    Google Scholar 

  • Gagné RJ (2004) A catalog of the cecidomyiidae (Diptera) of the world. M Entomol Soc Wash 25:1–408

    Google Scholar 

  • Gagné RJ and Jaschhof M (2021) A catalog of the Cecidomyiidae (Diptera) of the world. Fourth edition. Digital 762 pp.

  • Geng XS, Chen YJ, Shi J, Shu JP, Zhang W, Yan-Fen WU (2019) Biological characteristics of Aiolomorphus rhopaloides Walker on different bamboo species. J Appl Entomol-CN 56:220–226

    Google Scholar 

  • Gopko M, Mironova E, Pasternak A, Mikheev V, Taskinen J (2020) Parasite transmission in aquatic ecosystems under temperature change: effects of host activity and elimination of parasite larvae by filter-feeders. Oikos 129:131–1540

    Article  Google Scholar 

  • He SQ, Jiang CY, Guo R, Wang YP (2016) Parasitoids of Aiolomorphus rhopaloides Walker. For Pest and Dis-CN 35:1–8

    CAS  Google Scholar 

  • Hernández-López M, Hernández-Ortiz V, Castillo-Campos G, Fernandes GW (2021) Size matters: larger galls produced by Eutreta xanthochaeta (Diptera: Tephritidae) on Lippia myriocephala (Verbenaceae) predict lower rates of parasitic wasps. Arthropod Plant Interact 15:615–625

    Article  Google Scholar 

  • Ito M, Hijii N (2004) Roles of gall morphology in determining potential fecundity and avoidance of parasitoid attack in Aphelonyx glanduliferae. J for Res 9:93–100

    Article  Google Scholar 

  • Jia ZG, Lu Q, Guo BG, Zhao M, Lang YQ (2004) Progress in the study of psammophyte-Haloxylon. For Res-CN 17:125–132

    Google Scholar 

  • Joseph MB, Gentles M, Pearse IS (2011) The parasitoid community of Andricus quercuscalifornicus and its association with gall size, phenology, and location. Biodivers Conserv 20:203–216

    Article  Google Scholar 

  • Laszlo Z, Tothmeresz B (2013) The enemy hypothesis: correlates of gall morphology with parasitoid attack rates in two closely related rose cynipid galls. Bull Entomol Res 103:326–335

    Article  CAS  PubMed  Google Scholar 

  • Li F, Wu X, Wang P, Liang H, Wang X, Wang L, Zhang J (2012) The occurrence regularity of psyllid in Haloxylon spp and its influencing factors. Acta Ecol Sin-CH 32:2311–2319

    Article  Google Scholar 

  • Li FL, Li T, Su J, Yang S, Wang PL, Zhang JP (2016a) Temporal and spatial differences in gall induction on Haloxylon by Aceria haloxylonis (Acari: Eriophyidae) in the gurbantunggut Desert. Syst Appl Acarol 21:1670–1680

    Google Scholar 

  • Li Q, Wang C, Hu H-Y, Kostjukov VV, La Salle J, Zhu C-D (2016b) Descriptions of three new species of Dzhanokmenia (Hymenoptera: Eulophidae) from China. Zootaxa 4121:447–457

    Article  PubMed  Google Scholar 

  • Li Q, Dzhanokmen KA, Triapitsyn SV, Hu HY (2018) Parasitoids reared from galls of Stefaniola sp (Diptera, Cecidomyiidae) on Haloxylon spp. in China, with redescription of Mesopolobus quadrimaculatus Dzhanokmen (Chalcidoidea, Pteromalidae). Turk J Zool 42:263–268

    Google Scholar 

  • Ma CS, Gu ZD, He LP, Gao WL, Zeng XD, Li R, Zhang J (2013) Prevention Measures and Varieties of Injurious Insect in Haloxylon ammodendron community at Downstream of Shiyang river in arid desert region. J Gansu for Sci Tech-CN 39:38–41

    Google Scholar 

  • Mohammadi M (2003) Phenological relation of the pests associated with Saxaul plant in Abardeg area. Iran J Range and Des Res 10(17–38):135–136

    Google Scholar 

  • Passos LC, Soares MA, Collares LJ, Malagoli I, Desneux N, Carvalho GA (2018) Lethal, sublethal and transgenerational effects of insecticides on Macrolophus basicornis, predator of Tuta absoluta. Entomol Gen 38:127–143

    Article  Google Scholar 

  • Plantard O, Hochberg ME (1998) Factors affecting parasitism in the oak galler Neuroterus quercusbaccarum (Hymenoptera: Cynipidae). Oikos 81:289–298

    Article  Google Scholar 

  • Quacchia A, Moriya S, Bosio G, Scapin I, Alma A (2008) Rearing, release and settlement prospect in Italy of Torymus sinensis, the biological control agent of the chestnut gall wasp Dryocosmus kuriphilus. Biocontrol 53:829–839

    Article  Google Scholar 

  • Saji A, Sakkir S, Dhaheri SSA (2013) Galling insects associated with Haloxylon spp. (Bunge) in Abu Dhabi, United Arab Emirates. Int J Biodivers Conserv 5:89–295

    Google Scholar 

  • Sardon-Gutierrez S, Gil-Tapetado D, Gomez JF, Nieves-Aldrey JL (2021) Ecological niche modelling of species of the rose gall wasp Diplolepis (Hymenoptera: Cynipidae) on the Iberian Peninsula. Eur J Entomol 118:31–45

    Article  Google Scholar 

  • Skovgard H, Nachman G (2015) Temperature-dependent functional response of Spalangia cameroni (Hymenoptera: Pteromalidae), a parasitoid of Stomoxys calcitrans (Diptera: Muscidae). Environ Entomol 44:90–99

    Article  CAS  PubMed  Google Scholar 

  • Skuhrava M, Karimpour Y, Sadeghi H, Gol A, Joghataie M (2014) Gall midges (Diptera: Cecidomyiidae) of Iran: annotated list and zoogeographical analysis. Acta Soc Zool Bohem 78:269–301

    Google Scholar 

  • Slepyan EI (1958) Specific characteristics of gall-forming and teratogenic processes on the assimilational shoots of Haloxylon aphyllum and H. persicum Chenopodiaceae referat. Bot Zhur 43:1595–1607

    Google Scholar 

  • Soares MA, Campos MR, Passos LC, Carvalho GA, Haro MM, Lavoir AV, Biondi A, Zappala L, Desneux N (2019) Botanical insecticide and natural enemies: a potential combination for pest management against Tuta absoluta. J Pest Sci 92:1433–1443

    Article  Google Scholar 

  • Spanoudis CG, Andreadis SS (2012) Temperature-dependent survival, development, and adult longevity of the koinobiont endoparasitoid Venturia canescens (Hymenoptera: Ichneumonidae) parasitizing Plodia interpunctella (Lepidoptera: Pyralidae). J Pest Sci 85:75–80

    Article  Google Scholar 

  • Stone GN, Schonrogge K (2003) The adaptive significance of insect gall morphology. Trends Ecol Evol 18:512–522

    Article  Google Scholar 

  • Tian QL, Liu T (2020) Relationship between the distribution characteristics of fine roots of Haloxylon persicum and soil moisture under extreme drought conditions. J Shihezi Univ (nat Sci) 38:80–87

    Google Scholar 

  • Wang JL, Lao GF, Li YW, Yang M, Mo ZQ, Dan XM (2018) Effects of temperature and host species on the life cycle of Cryptocaryon irritans. Aquaculture 485:49–52

    Article  Google Scholar 

  • Wu X, Zheng XJ, Li Y, Xu GQ (2019) Varying responses of two Haloxylon species to extreme drought and groundwater depth. Environ Exp Bot 158:63–72

    Article  Google Scholar 

  • Xiao H, Sun L, Jiao T, Li Z (2016) A revision of Chinese species of Mesopolobus Westwood (Hymenoptera: pteromalidae) with descriptions of four new species from China. Zool Syst 41:64–81

    Google Scholar 

  • Xu ZH, Hu GL, Jiang HZ, Ye YZ (2002) Ten species of Chalcidoids reared from bamboo gall with notes on one new record species. For Res-CN 15:444–449

    Google Scholar 

  • Xu R, Chen J, Wang X, Qiao HL, Peng F, XU CQ, Guo K, Liu TN, (2015) Occurrence and Control of the diseases and pests damage on Cistanche deserticola Y.C.Ma and its Host Haloxylon ammodendron. Mod Chin Med 17: 369-374

  • Xue XF, Zhang JP, Li FL, Hong XY (2012) A new eriophyoid mite species (Acari: Eriophyidae) infesting Haloxylon ammodendron and H. persicum (Chenopodiaceae) in Xinjiang Uigur autonomous region, northwest China. Syst Appl Acarol 17:202–209

    Google Scholar 

  • Zhao Q, Jiang LL, Guo J, Zhang DK, Hu HY (2021) Differences in gall induction of flower-like galls on Haloxylon by psyllids (Hemiptera: Aphalaridae), and the emergence of corresponding parasitoids. Insects 12:861

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We are grateful to Prof. Ke-long Jiao who is an expert taxonomist on Cecidomyiidae (Tianjin Agricultural University) for the identification of four Cecidomyiidae species. We also thank doctoral student Ning Kang (College of Life Science and Technology, Xinjiang University) and Qian Zhao’s husband Post-doc, and Jiao-Hong Li for editing the manuscript.

Funding

This research was funded by the National Natural Science Foundation of China (31672338 & U1170305), Tianshan Talent Project of the Xinjiang Uighur Autonomous Region (10020000220), and the Doctoral Innovation Project of Xinjiang University, China (XJUBSCX-2017018).

Author information

Authors and Affiliations

  1. Xinjiang Key Laboratory of Biological Resources and Genetic Engineering, College of Life Science and Technology, Xinjiang University, Urumqi, 830046, People’s Republic of China

    Qian Zhao, Dong-kang Zhang, Ling-ling Jiang, Jie Guo & Hong-ying Hu

Authors
  1. Qian Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dong-kang Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ling-ling Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jie Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hong-ying Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hong-ying Hu.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 32 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhao, Q., Zhang, Dk., Jiang, Ll. et al. Globular galls on Haloxylon (Centrospermae: Chenopodiaceae) induced by gall midges, and the corresponding parasitoids in China. Appl Entomol Zool 58, 345–356 (2023). https://doi.org/10.1007/s13355-023-00840-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13355-023-00840-x

Keywords

Search

Navigation