Insecta, Linnaeus, 1758

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 : 20-22

4.3. Oothecae in Insecta

The original definition of ootheca according to Snodgrass (1993) suggested that the oothecal material originates from some part of the female genital tract, most often from modified accessory glands. However, Nichols and Schuh (1989) classified the protective egg batch cover in Plataspidae as oothecae despite the fact that the material originates from the female digestive tract. It is clear that the definition of oothecae either by source or by product is not entirely overlapping and should be adjusted to avoid misunderstandings. Henceforth, any female-derived structures tightly spatially connected with genital or digestive tracts or any structures protecting eggs, regardless of endogenous or exogenous origin, and immediately placed on the eggs during the oviposition, reported by various authors under different terms, are classified here as an ootheca.

Table 1 contains occurrences of oothecae in insects, including silk cocoons and spumaline secretions summarized by Chapman (2013) and mentioned also by other authors, brochosomes ( Rakitov, 1999), wax (e. g., Eiseman and Charney, 2010), and resin ( Forero et al., 2011). The following outline highlights similarities and differences in ootheca location, source and composition of oothecal material, features of oothecae, and their occurrence across insects. When papers with respective information are listed in Table 1, they are not cited in the following text.

4.3.1. Location of the ootheca

Females usually deposit oothecae on or close to a source of larval food, most frequently on different parts of plants, i.e., on bark either of twigs or stems ( Mantodea ; Phasmatodea; Psocodea ; Hemiptera : Heteroptera : Reduviidae : Phymatinae, some of Harpactorinae; Plataspidae ; Auchenorrhyncha: Aethalionidae , Fulgoridae , Issidae ; Sternorrhyncha: some Coccoidea; Coleoptera : Buprestidae ; Lepidoptera : Lasiocampidae , Erebidae : Lymantriinae – often on the female cocoons, Tortricidae ; Diptera : Asilidae ), on leaves ( Mantodea ; some of Harpactorinae (including Apiomerini); Auchenorrhyncha: Aethalionidae , Cicadellidae : Cicadellinae ; Sternorrhyncha: Aleyrodoidea, Aphidoidea; Coleoptera : Chrysomelidae : Cassidinae, Donaciinae, Curculionidae ; Tortricidae ), underneath bark or in bark crevices ( Mantodea ; Heteroptera : Urostylididae ; Auchenorrhyncha: Fulgoridae , Issidae , Membracidae ), or on roots of plants (Sternorrhyncha: some Coccoidea), within silk galleries on various substrate ( Embioptera ). In addition, oothecae may be deposited in soil (some of Mantodea ; Caelifera; Mantophasmatodea ; Sternorrhyncha: some Coccoidea) or on top of soil/substratum ( Mantodea ; Blattodea including Isoptera; rarely Caelifera, some of Harpactorinae), in water ( Ephemeroptera – on submerged objects; Odonata – on submerged objects and plants; Coleoptera : Hydrophilidae – freely floating or on floating objects, Psephenidae – on submerged objects; Trichoptera – on submerged objects; Diptera : Chironomidae – freely floating, rarely on submerged objects, Ceratopogonidae – on vegetation, Chaoboridae – freely floating, Dixidae – attached to solid substrate) or on vegetation and/or objects overhanging water ( Megaloptera : Corydalidae ; Neuroptera : Sisyridae – often in depression or crevice; some of Trichoptera ).

Females of Mantodea, Caelifera and Mantophasmatodea actively prepare the location of the ootheca by digging a furrow ( Mantodea ) or hole (the remaining mentioned above) into the substrate. In some Membracidae (Auchenorrhyncha) , females slice the bark with their ovipositor, deposit eggs and cover them with oothecal secretions. Females of Proconiini ( Cicadellidae ) oviposit eggs by identical way on living plant leaves. Females of Iris Saussure ( Mantodea : Tarachodidae ) guard the ootheca until larvae hatch ( Costa 2006) and those of non-termite Blattodea and Hydrophilidae even carry the ootheca attached to the abdomen until shortly before larvae hatch.

4.3.2. Origin of the oothecal material

In most of the insects, oothecal substances are produced in the female genital tract, most commonly in modified accessory glands. Often called colleterial glands, they are of ectodermal origin and open into the ectodermal part of the internal female genitalia, e.g., the common oviduct, gynatrium or vagina. In those instances where oothecal secretions are derived from mesodermal glands these glands are called pseudocolleterial glands and open, e.g., on the distal part of the lateral oviduct (Caelifera are the best example – Hinton, 1981).

Colleterial glands have been documented in Mantodea , Blattodea including Isoptera, and in most of Reduviidae (subrectal and other glands; Weirauch, 2008). Oothecal secretions are produced from diverse colleterial glands in Membracidae , Issidae , Corydalidae , Hydrophilidae , Donaciinae, Trichoptera , Lasiocampidae , Lymantriinae , Tortricidae , Chironomidae , Ceratopogonidae , Chaoboridae , Dixidae , Asilidae , very probably also in Sisyridae and Psephenidae , and this origin is assumed in Mantophasmatodea . The pseudocolleterial glands are functional in Urostylididae , and both the colleterial and pseudocolleterial glands in Caelifera, Buprestidae and Cassidinae. Oothecal material originates from fibrillar matrix of egg exochorion produced by follicle cells in Ephemeroptera and Odonata .

Although the origin of secretion of ootheca is not known in Phasmatodea, Aethalionidae , Fulgoridae and Curculionidae , the oothecal material in Psocodea and Plataspidae originates from part of digestive tract, either from one pair of modified labial glands ( Psocodea ) or from modified epithelium of posterior part of midgut ( Plataspidae ). Material of ootheca can be also produced by silk glands situated in front tarsi in Embioptera , by modified segment of Malphigian tubules (secretion called brochosomes) in Proconiini ( Cicadellidae ), and by dermal wax glands in Sternorrhyncha. Resin from plants composes oothecal material in Apiomerini ( Reduviidae ).

4.3.3. Chemical composition of the ootheca

Details of the composition of oothecal material are so far unavailable for Ephemeroptera , Odonata , Mantophasmatodea (described as “cementing material”), Phasmatodea, Harpactorinae (except Apiomerini), Phymatinae, Plataspidae , Aethalionidae , Fulgoridae , Issidae (mentioned as “cottonlike secretion”), Corydalidae , Psephenidae ,

Donaciinae, and Curculionidae . Comprehensive analyses of the composition of the secretion that forms the oothecae have been conducted only for some taxa (in parentheses in the following text), while the approximate composition is known more frequently.

In those taxa for which detailed composition profiles have been established, the secretion is often proteinaceous, i.e., Blattodea including Isoptera (mostly sclerotin), Embioptera, Caelifera , Psocodea , Sisyridae , Hydrophilidae (fibroprotein sericin, component of silk, eventually plus cementing substance), Buprestidae , Chrysomelidae – Cassidinae, and Asilidae (probably albumin).

Proteins (α- helical) are also important components of oothecal material in Mantodea with added calcium-based compounds and enzymes. The oothecal substance is composed from proteins, saccharides and lipids in Membracidae , and from proteins and lipids in Proconiini . Complex polysaccharides, another main component of oothecal material, with added proteins are known in Urostylididae , and substance with similar composition is termed spumaline: from complex polysaccharides in Trichoptera , Lasiocampidae , Lymantriinae , Tortricidae , from mucopolysaccharides in Chironomidae , Ceratopogonidae , Chaoboridae and Dixidae . Wax of Sternorrhyncha is composed from esters of fatty acids and of long-chain alcohols, and resin used by Apiomerini is viscous mixture of organic components, mostly terpenes.

4.3.4. Structure and shape of the ootheca

Although details of the shape and structure of oothecae are highly diverse across insects, they can roughly be subdivided into hardened and gelatinous structures.

Hardened structures. The most familiar and elaborate ootheca in this category is the ootheca in Blattodea including Isoptera. The rigid, tanned, sclerotized ootheca with two rows of six to fifty eggs is formed inside the female vestibulum and hardens outside the gonopore in most of the non-termite Blattodea and in one member of the Blattodea : Isoptera, the earliest diverging lineage Mastotermes darwiniensis Froggatt , where the ootheca, with up to 24 eggs, bears irregular appendage of variable size at the proximal end. An ootheca from harden froth with up to 400 eggs of complex detailed structure and variable shapes is produced by Mantodea .

Additional taxa have oothecae in the form of a hard structure, i.e., Phasmatodea, some Harpactorinae, Phymatinae, Plataspidae , Membracidae , Corydalidae , Buprestidae , Lasiocampidae and Asilidae . The oval ootheca either completely encloses up to 34 eggs in Phasmatodea, or leaves only opercula of numerous eggs visible in both reduviid taxa or completely covers up to 53 eggs in Plataspidae in shape of roof. In Membracidae , the ootheca covers numerous eggs and oothecal secretions contain attractants for other females to oviposit on the same place resulting in large clumps of egg masses and thus ensuring better attendance and tendance by the ants (e.g., Gibernau and Dejean, 2001; Perotto et al., 2002). The flat ootheca of Corydalidae covers up to 1000 eggs, whereas only one or few eggs are contained in the globular ootheca of Buprestidae , and numerous eggs in the oval ootheca of Lasiocampidae and Asilidae .

The coleopteran taxa Cassidinae and Curculionidae produce a specific type of ootheca – complex, compact, translucent, slightly convex or oval, with each egg (from one up to 100 in Cassidinae, up to 15 in Curculionidae ) enclosed in double membranes. Hydrophilidae construct a highly specific, oval or spherical ootheca with mast, containing mostly 100 eggs. A web or sheet of silk threads covers the mass of eggs in Psocodea and Sisyridae , forming white patches and flattened structure, respectively. Embioptera cover up to 100 eggs with silk mixed with bits of bark, macerated lichens and frass inside galleries.

Hard structure from mass of ultramicroscopic structures = brochosomes, called “white chalky material”, covers eggs (up to about 21) inserted to slits made by female in plant leaf in Proconiini . Hard wax structures of various shape protect eggs (up to 100) in Sternorrhyncha. Those females use different way of oviposition behaviour, i.e., i) oviposit eggs in spirals on abaxial side of plant leaves and covered them with wax (Aleyrodoidea), or ii) produce so-called ovisac by transferring fine wax threads to mass of eggs on leaves (Aphidoidea) and various parts of plants (Coccoidea), or have wax ovisac attached to abdomen of female ( Margarodidae , Ortheziidae ).

The hardened ootheca is often not only formed by the female’ s secretions but also incorporates external materials. Caelifera and Mantophasmatodea construct a cylindrical ootheca from frothy secretion and from soil particles or sand grains with up to 200 eggs in Caelifera and up to 30 eggs in Mantophasmatodea . Females of three auchenorrhynchan families, Aethalionidae , Fulgoridae and Issidae , construct oothecae from their secretions in combination with fine grains of soil or sand, or with clay or mud. Aethalionidae produce a semiglobular ootheca with around 100 eggs, around 40 eggs with visible outlines are in Fulgoridae ootheca, and up to 22 eggs in spike-shaped ootheca in Issidae . The lepidopteran taxa Lymantriinae and Tortricidae mix hardening spumaline with hairs or scales from the females, covering up to 300 ( Lymantriinae ) or up to 400 ( Tortricidae ) eggs.

Gelatinous structures. Sticky or gelatinous oothecae are less obvious and common. In Ephemeroptera , eggs are covered with a semitransparent thick jelly coating, while in Odonata , masses of eggs are deposited in a jellylike substance that incorporates debris and forms a semitransparent coating. Numerous eggs are covered with firm, viscous in Apiomerini respectively, sticky secretion in Harpactorinae, and similarly in Urostylididae the eggs are almost entirely embedded in a jellylike substance. Psephenidae oviposit up to 1000 eggs in a single layer covered with jellylike substance. A concentric arc of eggs surrounding a hole in a leaf is covered with transparent gelatinous material in some Donaciinae. Several Trichoptera cover eggs with transparent spumaline and glued to leaves. Rope-shaped masses of numerous eggs are embedded in transparent gelatinous spumaline swelling in water in Trichoptera and in Chironomidae , eggs are arranged spirally in egg rafts forming floating discs covered with gelatinous material in Chaoboridae (up to 350), and masses of eggs are deposited in a gelatinous matrix in Ceratopogonidae and Dixidae .

4.3.5. Systematic occurrence of the ootheca within Insecta

It is clear that oothecae occur in numerous lineages of insects. However, an evaluation of their evolutionary origins across insects will need to await more refined phylogenetic hypotheses in many groups.

A jellylike substance covering batches with a high number of eggs occurs in Ephemeroptera and Odonata with an exophytic type of eggs. A sister group relationship of Ephemeroptera and Odonata , constituting the Palaeoptera, is currently the best-supported hypothesis from a morphological as well as a molecular point of view (Misof et al., 2014; Simon et al., 2018). This could indicate that a jellylike egg cover may have originated in the common ancestor of the group. However, jellylike egg covers also occur in other insect taxa that deposit eggs in water, e.g., members of the Culicomorpha, where they are independently derived, suggesting that this feature is an adaptation to oviposition in water that may have evolved multiple times independently. Nevertheless, in both Ephemeroptera and Odonata the oothecal secretion originates from follicle cells representing a unique pattern among Insecta ( Gaino and Rebora, 2001; Gaino et al., 2008), and we therefore hypothesize that the jellylike egg cover could be a synapomorphy for Palaeoptera.

The presence of an ootheca has so far been used as evidence in a phylogenetic framework only in Dictyoptera, where it is thought to be synapomorphic for the entire group ( Nalepa and Lenz, 2000; H¨ornig et al., 2013; 2018; Evangelista et al., 2019). Fossil oothecae are rare but known (e.g., H¨ornig et al., 2018; Gao et al., 2019; Li and Huang, 2019; Cariglino et al., 2020). Mantodea feature a relatively longer ovipositor compared to other dictyopterans and the complicated ootheca is assembled outside the body in using a complex behavioural sequences (Hornig ¨et al., 2013). In contrast, the ootheca in Blattodea (incl. one species of Isoptera) is constructed in the female vestibulum. In non-termite Blattodea , the fully formed ootheca is then frequently carried by the females using the gonopore for some time, supported by the gonapophyses. The ootheca of Isoptera has a simpler structure than the ootheca of other blattodean groups, with the parsimonious explanation inferring that this is due to secondary reduction according to Nalepa and Lenz (2000). Within Dictyoptera, it is generally assumed that the construction of a blattodean-type ootheca is connected with the development of a short ovipositor (facilitating production of free oothecae and active maternal transport) (e.g., Evangelista et al., 2019), although according to Hornig ¨et al. (2013, 2018) and supported by Cariglino et al. (2020) the ancestral ootheca in Dictyoptera was more likely constructed using an ovipositor-type (i.e., externally visible) still found in modern Mantodea .

Among the remaining Polyneoptera, oothecae are known in the Embioptera, Phasmatodea , Mantophasmatodea and Caelifera ( Orthoptera ). All stages and both sexes of Embioptera spin galleries from silk on substrate ( McMillan et al., 2016). Females cover either egg mass or single eggs with silk to produce cocoonlike ootheca separated from interior of silk tunnel. The ootheca in one species of Phasmatodea was discovered only very recently. Females of the Phasmatodea mostly produce eggs with a thick chorion singly to avoid aggregation of hatched larvae, but egg protection using an ootheca may be more common than is currently known ( Goldberg et al., 2015; Robertson et al., 2018). The females of Mantophasmatodea and Caelifera oviposit their eggs similarly, where foam secretion together with the substrate harden into an egg pod with a froth plug. While the existence of an ootheca in Mantophasmatodea has been explained as protection against desiccation in dry environmental conditions (e.g., Eberhard, 2009), females of Caelifera build the ootheca in various habitats, including dry and wet environments (e.g., Stauffer and Whitman, 2007). Du et al. (2022) consider ootheca as a convergence in egg-laying strategy across Polyneoptera which was adapted as a successful reproductive strategy of this taxon. However, that conclusion was based only on study of non-termite Blattodea , Mantophasmatodea and Caelifera ( Orthoptera ).

Within Paraneoptera, structures protecting eggs are present in Psocodea and in Hemiptera . Psocodea have several types of eggs, where one type of batches of eggs with relatively thin chorion is covered with silk threads. Hemiptera includes Sternorrhyncha, Auchenorrhyncha, Coleorrhyncha and Heteroptera . Oothecae of slightly different construction than in Psocodea have been described in five auchenorrhynchan families (e.g., Boulard, 1987; Wood and Keese, 1990; Azevedo-Filho and Carvalho, 2005; Rando and Lima, 2010; Malek et al., 2019) and in three taxa of Sternorrhyncha (e.g., Eiseman and Charney, 2010). In Membracidae (Auchenorrhyncha) , the ootheca is closely connected with trophobiosis with ants (e.g., Wood, 1982). Different groups of Sternorrhyncha protect eggs by wax structures, often called ovisac.

Based on the occurrence of the ootheca in Heteroptera (see above) and Auchenorrhyncha, Tallamy and Schaefer (1997) suggested that a hemipteran common ancestor already showed a tendency for egg protection. However, oothecae certainly evolved multiple times independently within Hemiptera , since recent taxa that produce oothecae are not particularly closely related.

Our knowledge on the occurrence of oothecae within Holometabola is very scattered, in part because of the large number of species involved. Within Neuropterida, females of the megalopteran family Corydalidae construct distinct oothecae protecting their eggs from excessive heat ( Mangan, 1992), and females of the neuropteran family Sisyridae cover their eggs with silk sheets. In both families, eggs are laid on objects overhanging water, into which the hatching larvae fall.

Oothecae have been described for several taxa of Coleoptera , but they are very probably more widely distributed than currently documented. Hydrophilidae females construct oothecae in the water in shape of silk cocoon. Also, females in the family Psephenidae oviposit in water, where eggs are arranged in compact patches with gelatinous cover. The globe-shaped hard structure protects eggs in the Buprestidae . The females of two related taxa, Cassidinae and Curculionidae construct a similar, rather unique structure from up to 200 translucent membrane layers. Females of other chrysomelid taxon, Donaciinae, cover mass of eggs with jelly material.

Females of closely related Trichoptera and Lepidoptera cover their egg batches with spumaline. Oothecae remain gelatinous in Trichoptera , while they harden in Lepidoptera and their material is often mixed with setae or scales of females.

Within Diptera , females from several families within Culicomorpha construct oothecae. Their eggs are deposited in water and coated by spumaline. That behavioural pattern could probably be an adaptation to aquatic habitats. The only other known Diptera with oothecae is the family Asilidae , where the ootheca is firm, deposited not in water but on land. We have too little data about occurrence of ootheca in that large insect taxon, though it is clear that this structure developed several times independently.

Published data about the occurrence of oothecae within insects are rare, but it is almost certain that the protection of eggs by such structures is a much more widespread phenomenon than is presently known. Oothecae are likely highly adaptive structures that probably only make sense under specific environmental conditions. It does seem reasonable to assume that they may evolve as adaptations that facilitate the colonization of new environments, such as dry and hot habitats, where they likely protect eggs against desiccation, in addition to protection from predators and parasitoids ( Fatouros et al., 2020). However interestingly, egg parasitoids prefer to oviposit in eggs of Lycorma delicatula (White) within ootheca over in artificially uncovered eggs and hence benefit from this protection for its own progeny ( Malek et al., 2019).