Heteroptera (Tallamy and Schaefer, 1997)

Vilímová, Jitka, Weirauch, Christiane & Janšta, Petr, 2023, The ootheca of Libyaspis flavosparsa (Montandon) (Heteroptera: Plataspidae), with a review of ootheca-production in Heteroptera and other Insecta, Zoologischer Anzeiger 306, pp. 10-26 : 18-20

4.2. Oothecae in the Heteroptera

Oothecae are rare in Heteroptera and have so far only been documented for species in three families. Although often overlooked in accounts of oothecae in Heteroptera (e.g., Cobben, 1968), they likely occur in most species of the pentatomoid Urostylididae (Jing-Fu Tsai in lit.). Females of Urostylididae oviposit groups of eggs in differently shaped batches vertically or horizontally in bark crevices ( Kobayashi, 1965; Kobayashi and Tachikawa, 2004; Kaiwa et al., 2014). Eggs are almost entirely embedded in copious amounts of a jellylike substance composed particularly from polysaccharides, but the MPs remain free of this secretion. The jelly is produced by the proximal halves of the ovarioles and each egg is covered with it while passing through the ovariole. Bacterial symbionts that are produced in a specialized organ in the genital chamber are added to the jelly during oviposition. Uniquely, nymphs hatch during winter when food is unavailable and feed on oothecal material and symbionts up to the third instar. The ootheca has therefore not only a protective function, but is also a nutritional resource ( Kaiwa et al., 2014).

Within Reduviidae , oothecae have been documented for species in several genera of Harpactorinae, e.g., Rhynocoris Hahn , Sycanus Amyot and Serville , Zelus Fabricius , and Apiomerus Hahn , and in species of Phymata (Latreille) that belongs to the Phymatinae ( Kershaw, 1909; Davis, 1957; Miller, 1971; Vennison and Ambrose, 1990; Coscar´on et al., 1998; Wolf and Reid, 2000; Dellape´et al., 2002; Weirauch, 2006; Luo et al., 2010; Forero et al., 2011). In Harpactorinae, batches of vertically or horizontally deposited eggs are covered with large amounts of sticky, non-hardening female secretions, only leaving the opercular region exposed. The stickiness of these very simple oothecae may deter egg predators and limit access of egg parasitoids. In species of Zelus that belongs to a clade of Harpactorini where adults produce sticky traps for prey capture ( Zhang and Weirauch, 2014), early instar immatures use the female-derived sticky oothecal secretions to enhance prey capture before their sticky glands develop in later instars (e.g., Wolf and Reid, 2000; 2001; Zhang and Weirauch, 2011). Females of Apiomerus (Apiomerini) collect viscous resin from plants and deposite it on venter of their abdomen before oviposition. Later, they transfer resin to gonocoxae and gonapophyses and coated each egg during oviposition. Finally, the entire egg mass is covered except opercular region. Similarly as in Zelus , first instar nymphs accumulate resin after hatching on their protibiae to prey capture ( Forero et al., 2011; 2013). Females of Phymata (Phymatinae) also deposit their eggs enclosed in an ootheca ( Davis, 1957). In contrast to those in Harpactorinae, phymatine oothecae have a foamlike appearance when freshly deposited, but harden into a non-sticky cover where only the operculum of the egg remains visible (Masonick and Weirauch, unpublished data). Given the distant relationships of Harpactorinae and Phymatinae and the differences in oothecal texture, these protective structures are very likely non-homologous and may have evolved as adaptive traits following the transition from ground or tree bark-associated habitats to dwelling and ovipositing on the more exposed leafy parts of plants ( Hwang and Weirauch, 2012).

The evolution of oviposition patterns (egg batches, single eggs) and egg orientation (horizontal, vertical) across Heteroptera is likely complex and ancestral states for most clades have not been inferred based on phylogenetic hypotheses and formal ancestral state reconstructions. Cobben (1968) suggested that vertically deposited eggs are the derived condition within Heteroptera , representing an adaptation for optimizing oviposition space. If the horizontal pattern observed in Plataspidae represents a plesiomorphic or apomorphic arrangement within Pentatomoidea remains to be investigated. The weak left-right asymmetry of the freely deposited eggs has been speculated to be the result of a constraint by the oblique arrangement of eggs in spike-shaped batches. The tightly packed arrangement of eggs in the ootheca of L. flavosparsa may in turn be the result of a spatial or oothecal secretion constraint, ultimately allowing for a higher number of eggs per egg batch (up to 60 in Libyaspis ( Carayon, 1949) , versus up to 16 in Coptosoma species (Davidov´a-Vilímov´a, 1987) and up to 40 in Megacopta species ( Ren, 1984)). The ancestral oviposition pattern for Plataspidae remains to be inferred.

Oothecal material in Heteroptera is either derived from different female internal structures or collected from plants and may either remain viscous ( Reduviidae : Harpactorinae: Wolf and Reid, 2000, 2001; Weirauch, 2006; Forero et al., 2011; Urostylididae : Kobayashi, 1965) or harden after deposition ( Reduviidae : Phymatinae: Davis, 1957; Plataspidae : Carayon, 1952). While oothecae in Harpactorinae are thought to be produced in subrectal = colleterial glands ( Davis, 1969), those in Urostylididae are secreted from the parts of ovarioles = pseudocolleterial glands ( Kaiwa et al., 2014); the source of the oothecal material in Phymatinae is unknown. As currently known, it is only in Plataspidae among Heteroptera that the material for the ootheca originates from the digestive tract and not from the female genital tract ( Goodchild, 1963).

Intriguingly, the oothecal material has been documented to fulfil functions other than egg protection in at least some instances, i.e., prey capture in Reduviidae and nutrition and endosymbiont transfer in Urostylididae . We speculate that endosymbiont transfer may also be one of the functions of the plataspid ootheca. Given the distant relationship of Reduviidae and Pentatomoidea ( Weirauch et al., 2019), oothecae in these two clades are without doubt of separate evolutionary origins. The situation is less clear-cut in Plataspidae and Urostylididae that according to some phylogenetic hypotheses either form two early diverging lineages ( Grazia et al., 2008) or more advanced and not closely related taxa ( Liu et al., 2019) or Urostylididae is early divergent while Plataspidae more advanced lineage (Roca- Cusachs et al., 2022; Ye et al., 2022) within the Pentatomoidea . Oothecae are rare in Plataspidae and it is unknown if the species that produce them are basal within Plataspidae . Oothecae therefore may or may not be plesiomorphic for Urostylididae and Plataspidae .

Costs and benefits of ootheca construction have not been investigated for Plataspidae . We speculate that although more eggs are oviposited per ootheca compared to a freely deposited batch, oothecal material production is likely costly. In contrast, females depositing free egg batches will need to deposit more batches for the same number of eggs and in addition deposit separate endosymbiont capsules.

We also speculate that trophobiotic interaction with ants and oothecal production are mutually exclusive strategies to protect offspring in Plataspidae . Gibernau and Dejean (2001) and Dejean et al. (2000 b, 2002) described trophobiosis in C. rugosa and pointed out that colonies of an unidentified species of Libyaspis living on the same tree were never attended by ants. Unfortunately, information on egg batches in this species were not provided ( Dejean et al., 2002; Dejean and Gibernau in lit.).