Hymenoptera

Ward, Anna K. G., Busbee, Robert W., Chen, Rachel A., Davis, Charles K., Driscoe, Amanda L., Egan, Scott P., Goldberg, Bailey A. R., Hood, Glen Ray, Jones, Dylan G., Kranz, Adam J., Meadely-Dunphy, Shannon A., Milks, Alyson K., Ott, James R., Prior, Kirsten M., Sheikh, Sofia I., Shzu, Shih-An, Weinersmith, Kelly L., Zhang, Linyi, Zhang, Y. Miles & Forbes, Andrew A., 2022, Borneosa aspera, Zoological Studies 61 (57), pp. 1-30 : 15-17

( Hymenoptera : Chalcidoidea: Eurytomidae : Eurytominae )

4,170 individuals (mean = 62.2, range 1–1,605) reared from 67 gall types ( Table S1).

Summary of Natural History: Eurytoma in the Nearctic comprise a large (> 80 species) group of mostly parasitic wasps associated with a large diversity of insects across several orders ( Bugbee 1967). At least 10 Nearctic species have been reared from oak galls, but their direct hosts are often uncertain, and indeed some Palearctic species are confirmed to attack nongalling inquilines ( Redfern and Askew 1998). Some Eurytoma are also phytophagous, although no exclusive phytophages are known from oak galls ( Bugbee 1967). Though some Eurytoma are apparently endoparasites ( Redfern and Askew 1998), Eurytoma in other Cynipid galls, including oak galls in the Palearctic, are uniformly ectoparasites, with species in some galls feeding on the gall organ once the primary host insect has been exhausted ( Gómez et al. 2011).

Reported host ranges of oak gall-associated Eurytoma vary from a single species to more than 75 hosts ( Bugbee 1967; Gómez et al. 2011; Askew et al. 2013). However, the diversity of the Nearctic fauna has yet to be interrogated genetically, and those in the Palearctic only marginally so. One particularly generalist-appearing species in the Palearctic, Eurytoma brunniventris Ratzeburg , has shown some evidence of genetic structure at the COI locus, with specimens reared from five species of oak gall wasps sorting genetically by tree host section ( Ács et al. 2010). Until an integrative assessment of species limits can be performed for Nearctic Eurytoma , interpretation of their host ranges will likely remain limited.

Relationship to galler phylogeny: Eurytoma were or have previously been reared from most oak galls represented in the Nearctic gall wasp phylogeny ( Ward et al. 2022) ( Fig. 7a ). If they appear sparse anywhere on the phylogeny, it is among the Neuroterus part of the tree ( Fig. S1 ; tips 4–17), many of which were collected as small flower or leaf galls.

Biogeography and oak tree section: Eurytoma were reared from galls across all three floristic regions ( Fig. 7b ) and from 48–64% of gall types collected from each oak section ( Fig. 7c ).

Tree organ and gall size: Eurytoma were reared from galls on all oak organs studied ( Fig. 7d ) though were more often reared from larger galls (84%) than from small galls (29%; Fig. 7e ).

Co-occurrence with other natural enemies: Eurytoma were significantly more likely to be present when Ormyrus (P = 0.0033) or Torymus (P = 0.0200) wasps were also present ( Fig. 7f ). This may indicate a) b)

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overlap in the types of gall morphologies favored by each parasitoid genus.

Additional Notes: Like Ormyrus and Torymus , Eurytoma are near-ubiquitous in their association with oak galls: we reared them from 64 (52.5%) of the 122 gall types that had five or more insect specimens emerge ( Table S1). Also like these other genera, Eurytoma may be more species-rich than they currently appear, with each species more specialized on particular dimensions of gall environments ( Zhang et al. 2014). A thorough integrative analysis of this group will be necessary to address questions about their evolution, ecology, and taxonomy.

Figures

Fig. 7. Summary of data for Eurytoma collected from Nearctic galls. For full explanation of figure details, refer to figure 1 legend. a) Associations of Eurytoma with the Nearctic oak gall wasp phylogeny (Fig. S1). b) Gall types from which Eurytoma were reared in the Californian (blue), Mexican and Central American (orange), and Eastern North American (green) floristic provinces. c) Associations of Eurytoma with trees in sections Quercus (Q), Lobatae (L), and Virentes (V). d) Association of Eurytoma with gall types on different oak tissues. e) proportion of gall types of three size categories (“small” <0.5 mm; “medium”, “large”> 20 mm) from which Eurytoma were reared. f) Results of probabilistic co-occurrence analysis for Eurytoma against seven other common associates. Yellow = significantly less likely to co-occur; blue = significantly more likely to co-occur; gray = no difference from probabilistic expectations. g) Eurytoma lateral habitus.

Fig. 1. Summary of data for Synergus inquilines reared from Nearctic galls. a) Associations of Synergus mapped to the Ward et al. (2022) Nearctic oak gall wasp phylogeny (Fig. S1). Numbers at tips of branches refer to those in figure S1. Closed circles at branch tips indicate Synergus was reared from galls of that gall wasp species in this study. Open circles indicate other previously known associations either not studied by us or not recovered in our collections. Blue-colored branches within the phylogeny indicate Palearctic gall wasps. b) Total number of gall types from which Synergus were reared in the three bioregions identified by Hipp et al. (2018) as constituting different assemblages of North American oaks: Californian (blue), Mexican and Central American (orange), and Eastern North American (green) floristic provinces. Numbers in parentheses indicate the total number of gall types collected in each region, excluding gall types from which no insects emerged. For figures c–f, gall types from which fewer than five individual insects were reared were excluded, whether or not a Synergus was reared. c) Associations of Synergus with trees in sections Quercus (Q), Lobatae (L), and Virentes (V). Gray bars and numbers indicate gall types with which a Synergus was associated. White bars and numbers indicate the number of gall types from which a Synergus was not reared. d) Association of Synergus with gall types on different oak tissues. Clockwise from top left: leaf, stem, acorn, flower, petiole, bud (“Bud” includes galls that may be found on both buds or stems. “Petiole” includes galls that may be found on both petioles and stems or petioles and leaves); e) proportion of gall types of three size categories (“small” <0.5 mm; “medium”, “large”> 20 mm) from which Synergus were reared. f) Results of probabilistic co-occurrence analysis (Veech 2013) for Synergus against seven other common associates (Cer = Ceroptres, Euc = Euceroptres, Orm = Ormyrus, Syc = Sycophila, Tor = Torymus, Eur = Eurytoma, Eud = Euderus). Yellow = significantly less likely to co-occur; blue = significantly more likely to co-occur; gray = no difference from probabilistic expectations. g) Synergus lateral habitus.