Ischnodemus sabuleti

Gidó, Zsolt, 2025, Seasonal de-alation of the macropterous morph of the wing-dimorphic bug Ischnodemus sabuleti (Hemiptera: Heteroptera: Blissidae): accumulation of injuries or active autotomy?, Journal of Natural History 59 (5 - 8), pp. 475-496 : 479-493

Reproductive period of I. sabuleti in Hungary

According to the results of the dissections and field observations, the reproductive period of I. sabuleti in Hungary starts in April and lasts until mid-summer (early July), when the last members of the old generation pass away. The new adult generation starts to emerge in late July–early August. Usually, the old and new adult generations do not overlap.

None of the 15 macropterous and 15 brachypterous females collected 15 March 2024 contained mature eggs. There is no dissection data from April, but intensive courtship and copulation was observed on 16 April 2024. The majority of both macropterous and brachypterous females contained mature eggs from May to July, while no female collected from August to November contained any mature eggs. Also, no mating behaviour was observed during the late summer–autumn period.

This means that the majority of Hungarian I. sabuleti individuals that emerge as adults in August–September enter a long reproductive diapause until the next spring (both wing forms). In most years, a smaller part of most of the populations overwinters as late-instar nymphs (third, fourth, and fifth stages). This is a logical consequence of the prolonged egg-laying period of the species, from late April until mid-July. The latest cohorts emerging from the eggs laid in mid-summer cannot reach the adult stage before the decreasing temperature slows their development and they enter the winter diapause as nymphs. The adults that develop from overwintered nymphs have a much shorter reproductive diapause, if any. Usually, they emerge as adults until the end of May, and presumably reproduce in June–July. The latest date on which the author observed young, immature adults in early summer was 12 June (2022: Darány).

The seasonal occurrence of the full-winged and wing-mutilated macropters

The seasonal occurrence of the full-winged and broken-winged macropters is shown in Figures 4–6 for the three best-sampled sites and years ( Figure 4 : Darány, 2021; Figure 5 : Baranyahidvég, 2022; Figure 6 : Csörötnek, 2022). All populations contained a considerable number of brachypters, which are not shown on these diagrams. A very clear pattern can be seen in these figures.

All macropterous adults keep their wings intact during the autumn and during hibernation. The very occasional occurrence of some broken-winged adults in autumn is probably due to accidents rather than autotomy. Apparently broken-winged adults start to appear in April, and from May to July almost all macropterous adults are broken winged. Broken-winged adults of the old generation disappear in July, and the full-winged new generation emerges in August–September.

No differences between sexes can be seen in these diagrams. However, the occasional full-winged individuals found in early and mid-summer are more likely to be males than females. As they represent only a small fraction of the observed populations, this fact might be non-significant.

Sporadic data from other, less systematically monitored populations (not presented here) corroborate the pattern seen in these diagrams. However, there is a remarkable exception: on 12 June 2022, a large percentage of full-winged macropters was observed in two populations: in Felsőszentmárton 5 of the 11 macropterous males (45%) and 7 of the 16 macropterous females (44%) collected were full winged. On the same day in a small, isolated Glyceria spot in Darány, 12 of the 21 macropterous males (57%) and 16 of the 36 macropterous females (44%) collected were full winged. These individuals probably were freshly emerged adults. In Darány one of them was visibly immature, with soft, yellowish cuticule.

The numbers of full-winged and broken-winged macropters available in the collection of the Hungarian Natural History Museum are shown in Figure 7 . They exhibit a very similar pattern, with one remarkable difference: both the appearance and the disappearance of the broken-winged macropters is delayed by approximately one month. It is very tempting to attribute this difference to climate change; however, caution is advisable as the sampling method was very different: random collections from all over the country rather than continuous monitoring of particular sites.

Considering the photos of I. sabuleti uploaded to the iNaturalist website (www.inatur alist.org, date of the investigation: 8 April 2024), broken-winged macropters have been captured between April and July, which is fully consistent with the author’s own data.

Direct observation of the mass flight of I. sabuleti

Mass flight of thousands of I. sabuleti macropters was observed directly by the author on 30 and 31 August 2024 at Darány. The bugs migrated from the dried-out Glyceria stands to the persisting Glyceria stands on the northern part of the same dry lakebed. The mass flight started in the late afternoon around 4pm and lasted until around 6pm, when the shade of the nearby forest reached the Glyceria stand. The day experienced hot, sunny weather with temperatures well above 30°C, and without wind. The bugs kept flying low (not higher than 1 m above the vegetation) and landed frequently on plants after flying several metres. The flight direction seemed to be orientated from south to north, according to the location of the already dry and still persisting Glyceria stands.

Lack of a direct relationship between sexual behaviour and autotomy

Both brachypterous and macropterous individuals have been observed to copulate, so wing autotomy can either precede or follow the first copulation. According to the author’s sporadic observations, macropters do not necessarily engage in autotomy behaviour directly after ending copulation.

Discussion

Ischnodemus sabuleti : age-related accumulation of injuries, active autotomy or both?

At the present state of knowledge three possibilities must be considered:

(1) Most Ischnodemus sabuleti individuals entering the reproductive age undergo partial de-alation simply due to the accumulation of natural wing injuries. Wing-cleaning behaviour is not exaggerated during the spring, but normal wing-cleaning behaviour may result in breaking off pieces from the already damaged wings.

According to Honêk (1976), regarding macropters of the red firebug Pyrrhocoris apterus Linnaeus, 1758 ( Pyrrhocoridae ), the membrane tends to break off after the gonads have become active. Interestingly enough, this is the only record of the natural, partial de-alation in the vast literature of the Pyrrhocoris wing dimorphism – possibly a similar strange neglect as in the case of I. sabuleti . Active autotomy is not mentioned in the case of P. apterus .

To the author’s knowledge, no similar phenomenon has been described in Heteroptera. It is certainly not common that the vast majority of a heteropteran population becomes de-alated and flightless simply due to ageing and natural injuries.

Ischnodemus sabuleti is not a keen and strong flyer (see above), so wing overuse by flying is not very likely. However, Ischnodemus sabuleti lives and moves frequently in the restricted space of Glyceria leaf sheets, where natural wing injuries may be quite possible. It is even possible that the very high incidence of brachyptery in the Blissidae family is partly related to their adaptation to avoid unnecessary wing injuries when moving inside the leaf sheets. The low resilience of the forewing membranes of Ischnodemus sabuleti compared with the majority of heteropterans might be simply explained by the lack of selection pressure on keeping the flight ability during the reproductive phase (see the discussion of ‘oogenesis-flight syndrome’ below). This is more likely to be the case for Pyrrhocoris apterus , where macropters are non-fliers from the beginning.

However, if the membranes of I. sabuleti are so fragile, it is not easy to explain why the damage of wings is so rare during the late summer/autumn period when the bugs are very active, sometimes even taking flight. The only possible alternative to active autotomy is that the membranes lose their mechanical resilience during hibernation.

(2) Most Ischnodemus sabuleti individuals become de-alated by active wing autotomy (practiced with the hind legs) during the spring, but the autotomy is triggered mainly by the irritation caused by natural wing injuries. Once initiated, the autotomy behaviour becomes self-triggering, due to the continuous irritation caused by new injuries, and so rapidly leads to the total destruction of the hemielytral membranes and hindwings. Without initial injuries the wing autotomy is not triggered, which might explain why not all individuals undergo wing autotomy. Other key factors (eg photoperiod or hormonal changes) might play a mediating role: it is possible that the autotomy behaviour is blocked prior to hibernation even if natural injuries do occur. Otherwise, it is hard to explain the absence of wing autotomy in the late summer/autumn period.

(3) Most Ischnodemus sabuleti individuals become de-alated due to active wing autotomy (practiced with the hind legs) during the spring, even if their wings have no natural injuries. Wing autotomy is triggered by other factors such as photoperiod, host plant chemicals, hormonal changes, sex pheromones, etc.; the effect of natural wing injuries on wing autotomy is negligible.

Although de-alation without autotomy is unlikely for several reasons, at the present state of knowledge it cannot be excluded without further targeted observations. The question whether initial natural wing injuries do or do not play a key role in the induction of the wing autotomy of Ischnodemus sabuleti is entirely open. From an evolutionary perspective, injury-induced wing autotomy might be the initial phase from which injury-independent wing autotomy might evolve. Targeted observations and experiments are required to answer these questions.

The de-alation/wing autotomy of Ischnodemus sabuleti is probably an apomorphic, evolutionary ‘primitive’ phenomenon/behaviour

Wing autotomy is sporadically documented among true bugs (Heteroptera). According to the monograph of Schuh and Slater (1995), shedding of the wings is reported to be common in Enicocephalomorpha, Mesoveliidae and Veliidae , and to occur in some Aradidae . Torre-Bueno (1908) describes the wing autotomy of some gerrid genera formerly grouped together as Halobatinae : Rheumatobates , Metrobates , Trepobates and Trepobatopsis . To the author’s knowledge, no comprehensive work mentions any case of wing autotomy in the superfamily Lygaeoidea .

The above-mentioned families represent distant heteropteran lineages ( Li et al. 2012; Song et al. 2024). Enicocephalomorpha is a separate infraorder although it is related to the infraorder Gerromopha ( Song et al. 2024) . Mesoveliidae , Gerridae and ‘Veliidae’ belong to infraorder Gerromopha while Aradidae , Blissidae and Pyrrhocoridae belong to three separate superfamilies within the infraorder Pentatomorpha . Within the Gerromorpha, Gerridae and ‘Veliidae’ are closely related (‘Veliidae’ is not monophyletic) while Mesoveliidae represents a more distant lineage ( Armisén et al. 2022). These facts indicate that wing autotomy appeared several times independently among Heteroptera.

Wherever the autotomy process has been directly observed – Trepobates pictus (Herrich-Schaeffer, 1847) : Torre-Bueno (1908); Mesovelia spp. : Kanyukova and Egorov (2022) – the wings are shredded with the hind legs, as described here for I. sabuleti . The author suggests that the autotomy behaviour of the true bugs evolved several times independently, but that in each case it developed from the normal, widespread wing-cleaning behaviour of heteropterans.

Wing autotomy is fairly frequent in Gerromorpha ( Torre-Bueno 1908; Hungerford 1919; Jordan 1951; Zettel 2008; Kanyukova and Egorov 2022). Within the Gerridae + ‘Veliidae’ lineage the degree of the autotomy (the place where the wings are broken off) is known to be group specific ( Zettel 2008).

Less is known about the wing autotomy of the Enicocephalomorpha ( Fernandes and Weirauch 2015) and Aradidae , and the author could not find any relevant articles; they are probably hidden in the sea of specific taxonomic descriptions.

Further research is desperately needed to assess how often de-alation/wing autotomy occurs among other Ischnodemus spp. and among other blissid genera. As the de-alation/ wing autotomy of I. sabuleti has been overlooked for so long, even great surprises might occur. If this behaviour is indeed restricted to a single or only to a few species within Blissidae , that would mean it is very probably an apomorphic, evolutionarily novel character. It would be also interesting to know whether wing autotomy occurs in any other family of the superfamily Lygaeoidea .

Also, further research is needed to determine whether there is any difference among the I. sabuleti populations in the ratio of the macropters practicing wing autotomy. As no wide-ranging investigations have been carried out, it is possible that in some populations wing autotomy is not as universal as in the studied Hungarian populations. Some photos on the Internet taken in mid-summer showing full-winged I. sabuleti macropters corroborate this possibility. Populations on the borders of the species’ distribution area merit special attention.

The ‘primitive’ characters of the I. sabuleti autotomy also indicate that it is a relatively new, perhaps still evolving behaviour. The timing of the autotomy is not fixed in relation to the first copulation or oviposition. The irregular breaking line of the membrane and the similarly irregular hindwing damage is also a primitive character, as opposed to the preformed breaking line present on the membrane of Rheumatobates spp. ( Gerridae , Jordan 1951).

Ischnodemus sabuleti may be a good model species to study the mechanism and evolution of heteropteran wing autotomy. It is a common species and has a large geographical distribution, and in many populations macropters are fairly abundant. Only its feeding and hiding habits present some inconvenience for observers and experimenters in both the field and the laboratory. In captivity, fresh Glyceria pieces must be given to the bugs every 3–4 days, and their propensity to hide complicates direct observation. However, these inconveniences can be solved with proper equipment and methodology.

Heteropteran de-alation/wing autotomy and wing dimorphism: a new aspect of the ‘migratory syndrome’

Most (if not all!) known cases of heteropteran wing autotomy (with the possible exception of the Enicocephalomorha and Aradidae ) are shown by macropterous morphs of the wing-dimorphic species. For the wing autotomy in the infraorder Gerroidea this statement has been confirmed by H. Zettel (pers. comm.). D. Fairbairn formulated the so-called ‘migratory syndrome’ hypothesis for the gerrid bugs, which states that different aspects of the dispersal ability are strongly correlated with each other ( Fairbairn and Butler 1990; Fairbairn 1994; Fairbairn and Desranleau 2008). Monomorphic macropterous gerrid species are more willing to take flight than macropters of the wing-dimorphic species and less often histolyse their flight muscles. Matalin (2003) demonstrated that monomorphic macropterous species of the ground beetles ( Carabidae ) are stronger flyers than macropters of the wing-dimorphic species.

A new aspect of the migratory syndrome is presented here as a hypothesis: macropters of the wing-dimorphic heteropterans are much more likely to practice wing autotomy than monomorphic macropterous species. However, more detailed study is needed (including of the Enicocephalomorpha and Aradidae ) to confirm the validity of this statement.

It is important to emphasise that the relationship between wing dimorphism and wing autotomy does not apply to all insect groups: for example, in crickets ( Gryllidae ) the autotomy of the hindwings is also practiced by some monomorphic macropterous species such as Svercacheta siamensis (Chopard, 1961) (S. Tanaka, pers. comm.).

Wing autotomy and the seasonality of I. sabuleti dispersal flight

The seasonal aspect of I. sabuleti ’s de-alation/wing autotomy fits within a well-known tendency. In many insect species the adult life is divided into a pre-reproductive dispersing stage and a subsequent reproductive, non-dispersing stage ( Johnson 1969). Older, reproductive adults often histolyse their flight muscles, becoming flightless, to obtain proteins for gonad development. Known heteropteran examples of this so-called ‘oogenesis-flight syndrome’ include gerrids ( Kaitala and Huldén 1990; Fairbairn and Desranleau 2008); pyrrhocorids: Pyrrhocoris apterus ( Socha and Sula, 2006, 2008) and Dysdercus cingulatus (Fabricius, 1775) ( Nair and Prabhu 1985) ; the lygaeid Horvathiolus gibbicollis (Costa, 1882) ( Solbreck 1986); and the rhopalid Jadera haematoloma (Herrich-Schaffer, 1847) ( Carroll et al. 2003) . Both macropters of wing-dimorphic species and monomorphic macropterous species are represented among the above-cited examples.

Like many other heteropterans, macropters of I. sabuleti use flight only for long-distance dispersal. They fly to colonise distant host plant stands, while they frequently transfer from one individual host plant to the other by walking. The main host plants of I. sabuleti are the mannagrass species ( Glyceria spp. ) in inland marshlands and the Elymus and Ammophila spp. on seaside dunes ( Tischler 1960). These plants usually form dense, homogeneous stands. Both adults (regardless of the wing form) and nymphs can walk easily from one plant to the other even in Glyceria stands occurring in water. They can use the criss-crossing, overlapping leaves as a transfer route, but they can also walk short distances on the surface of the water. Ischnodemus sabuleti bugs might cover fairly large distances by walking in herbaceous vegetation, and probably they can use also some nonhost plant species as occasional food and water sources.

Long-distance dispersal becomes essential when the host plant patch dies out. At least in the case of Glyceria maxima (Hart)Holm stands, this is a rather common phenomenon. Glyceria maxima prefers habitats which are usually characterised by changing water levels. According to the author’s observations, severe droughts often cause the dyingout of Glyceria stands. Less frequently, even long-lasting high water levels may eliminate mannagrass patches. In the case of drought, less-hygrophilous competitors such as Urtica, Polygonum and Bidens species are involved in eliminating the mannagrass. Sometimes, the Glyceria stands may be killed by large gradations of I. sabuleti itself, but more often the gradation of the bugs merely amplifies the devastating effect of the drought on Glyceria ( Gidó and Lehoczky 2023) .

To the author’s knowledge, there is no detailed information on the flight period of I. sabuleti . The seasonality of the wing autotomy (together with the suitable temperatures) allows a long dispersal period during late summer–autumn and another, shorter one in early spring. During late spring–early summer the overwhelming majority of I. sabuleti individuals are no longer able to fly, due to the de-alation of the macropters. While migration during late summer has been directly observed (see above), to the author’s knowledge there are no direct observations of migration by flight in early spring. Ischnodemus sabuleti seems to require high temperatures to fly, and unlike in August– September, hot days are not common during March–early April in Hungary. More empirical data is needed to clarify the seasonality of the dispersal flight of I. sabuleti .

Hypotheses on the supposed adaptive value of the wing autotomy of I. sabuleti and possibly also of other heteropteran species

It is unknown whether the supposed wing autotomy of I. sabuleti has any adaptive value. The simplest explanation is that the forewing membranes and the hindwings become dysfunctional as the insect enters the reproductive phase, and the removal of these mechanically vulnerable parts by ‘cleaning’ movements is neutral or, rather, slightly advantageous from the perspective of adaptation. However, other (secondary?) adaptive functions are still possible, especially in the cases of more advanced wing autotomy practiced by some gerroid bugs.

Torre-Bueno (1908) argues, discussing the wing autotomy of Rheumatobates and Trepobates spp. , that the membranes of macropterous females represent a mechanical obstacle to copulation, while those of the males hinder the locomotion of the copulating pair on the water surface. The present author finds these explanations rather unconvincing, and they certainly do not apply to I. sabuleti . Ischnodemus sabuleti does not inhabit the water surface, and even two macropters often copulate without any difficulties.

Some other testable hypotheses are presented below in detail; they are mutually non-exclusive.

One might speculate that if some insect predators or parasitoid wasps frequently grab the forewing membranes of I. sabuleti when attacking, then the removal of the membranes might help the bugs to escape some predatory attacks, as it is harder for the predator to grab the de-alated bug with the mandibles. At the present state of knowledge nothing more can be said about this possibility. To the author’s knowledge there are no parasites that attach themselves to the forewing membranes or to the hindwings, so it is unlikely that the autotomy serves the removal of parasites.

Another possibility is that the the brachypters and de-alated macropters, with their exposed black abdominal tergites, can absorb the solar radiation more effectively than the full-winged macropters. Ischnodemus sabuleti is known to be a heat-loving bug. It is possible that full-winged macropters need to spend a longer time sunbathing, during which they are more exposed to predators/parasitoids, while brachypters and de-alated macropters might be able to spend more time hiding inside the leaf sheets. This possibility certainly merits empirical testing.

The ‘wing muscle hypothesis’ has been tested on several other insect species, including the heteropteran red firebug Pyrrhocoris apterus . If autotomy/de-alation is the key stimulus for the flight muscle histolysis, which enhances the gonad development (‘oogenesis-flight syndrome’), then it is easy to attribute an adaptive advantage to the wing autotomy. However, there is no convincing evidence regarding a causal relationship between the de-alation and wing muscle histolysis. One (not decisive) counter-argument is that flight muscle histolysis is fairly common in many species, even in the absence of any de-alation. Some heteropteran examples of this: Gerridae ( Kaitala and Huldén 1990; Fairbairn and Desranleau 2008); Pyrrhocoridae : Dysdercus cingulatus ( Nair and Prabhu 1985) ; Lygaeidae : Horvathiolus gibbicollis ( Solbreck 1986) Rhopalidae : Jadera haematoloma ( Carroll et al. 2003) .

The effects of natural and artificial de-alation have mostly been studied in crickets ( Orthoptera : Gryllidae ) and the main results are reviewed by Tanaka (1994). Some species of crickets usually shed their hindwings after an initial period, but other cricket species do not. Natural wing autotomy of the crickets usually occurs somewhat after they start ovipositing, in some cases even after the peak oviposition period. In some crickets – including even species in which natural de-alation is unknown – artificial de-alation induces flight muscle histolysis and rapid egg production. However, different injuries (other than de-alation) are known to produce a similar effect in some other insect species: for example, the amputation of some legs induces precocious sexual maturity in the migratory locust Schistocerca gregaria Forsskål, 1775 . Tanaka (1994) concludes that the natural de-alation in the crickets is a consequence rather than a causative factor of the transition from the migrating life period to the reproductive life period.

Some relevant research has been conducted on the heteropteran Pyrrhocoris apterus , but the results are not conclusive. Artificial de-alation of macropterous P. apterus right at the beginning of the adult stage causes the significant shortening of the pre-oviposition period ( Socha 2007). Simultaneously, de-alation also accelerates the histolysis of the flight muscles ( Socha and Šula 2008). However – as is known in some other insects as well – other, different injuries, including sham operations, have a similar effect on P. apterus macropters ( Hodková and Socha 2006; Socha and Šula 2008). The injury signal is transmitted to the neuroendocrine complex via the nervous system. It induces the higher food intake necessary for repairing and healing of the injured tissues, and subsequently removes the inhibition of the corpus allatus, which was temporarily suppressed in spontaneously fasting macropterous adults via the nervous connections from the brain ( Hodková and Socha 2006; Socha 2007). It is important to note that in P. apterus de-alation has a much stronger effect on flight muscle histolysis than do sham operations ( Socha and Šula 2008). It would be interesting to learn how specific the physiological effect is of de-alation on flight muscle histolysis and gonad development.

The author suggests that in the case of I. sabuleti (and perhaps also in the case of the other heteropterans) it is unlikely that the wing muscle histolysis is the single or the most important adaptive function of the wing autotomy behaviour. However, it is definitely interesting enough to call for further research.

The ‘plastic surgery hypothesis’ of heteropteran wing autotomy is formulated here for the first time. It states that the de-alated macropters mimic the sexually more attractive brachypters to improve their reproductive fitness. The ‘plastic surgery hypothesis’ relies on the sexual selection theory and includes three basic assumptions:

(a) Brachypterous individuals are sexually more attractive than macropterous individuals.

(b) Greater sexual attractiveness results in higher offspring number and/or quality and thus in greater evolutionary fitness.

(c) Courting bugs often misidentify de-alated macropters as brachypters.

All three assumptions should be tested separately for both sexes, but might be sufficient if they are true for only for one of the sexes. (Characters which are functional only in one of the sexes might be expressed in another sex as well, due to rules of inheritance, eg men’s nipples).

The probability of these assumptions is briefly discussed below, using the sporadic facts published on these topics.

(a) It is generally held that among the wing-dimorphic insects the brachypterous form has a reproductive advantage over the macropterous form. Considering only the Heteroptera, this topic has been recently reviewed by Gidó (2023a, 2023b). It is important to note that the reproductive advantage of the brachypters in Heteroptera almost always manifests in the earlier sexual maturation of both sexes, but the lifelong fecundity of the brachypters is not always greater than those of the macropters. In the Blissidae family, much data is available on Cavelerius saccharivorus (Okajima, 1922) . Both female and male brachypters start reproducing earlier than the macropters ( Fujisaki 1986, 1992). However, the lifelong fecundity is a more complex matter in C. saccharivorus . This species is trimorphic, with two types of brachypters: ‘normal’ and ‘extreme’ brachypters. Macropters produce fewer eggs than the ‘extreme’ brachypters, but more than the ‘normal’ brachypters ( Fujisaki 1986). Not much data is available for I. sabuleti specifically, but Tischler (1963) states that brachypterous females contained mature eggs in May (North Germany), unlike the macropterous females collected at the same time. So, it is very likely that I. sabuleti brachypters also mature earlier than the macropters, while nothing is known yet about the lifelong fecundity of the two wing forms.

The reproductive advantage of the brachypters does not necessarily imply that they are preferred as sexual partners over the macropters. However, there is also some direct heteropteran evidence supporting the greater sexual attractiveness of the brachypters. Among the Gerridae + ‘Veliidae’ lineage, mating superiority of the non-macropterous males has been explicitly demonstrated in Aquarius remigis (Say, 1832) ( Kaitala and Dingle 1993) and Microvelia horvathi Lundblad, 1933 ( Matsushima and Yokoi 2022). In the latter case, the mating success of the brachypterous males was only slightly higher, but the brachypterous females proved to be both more attractive and more receptive than their macropterous conspecifics. In the case of Pyrrhocoris apterus , brachypterous females are also more receptive, and copulate more often than macropters do ( Socha 2004). There is a more complex, highly interesting pattern among the males: young brachypterous males are more successful in mating than macropterous young males; however, the opposite is true among old males (Socha 2006).

To the author’s knowledge there is no data on the differences in the sexual attractiveness between the two wing forms of any blissid species, including I. sabuleti .

(b) If there is no evidence, there are at least some hints that greater sexual attractiveness might result in greater offspring number/quality in Pyrrhocoris apterus .

(Although this is a plausible general assumption at least for the males, it shouldn’t be treated as self-understanding, especially not in invertebrates!). According to data presented by Socha (2008), only 3.21–76.46% (average 43.1%) of the eggs of receptive virgin females copulating with a single male for 120 min hatched, which the author considered fertilisation success. This means that a female can increase her fertility if she copulates more than one time. The choice among available male partners clearly influences both the fertilisation success and the offspring quality, and of course, a popular female can be much choosier. While the more attractive brachypterous females in fact are more receptive (see above), nothing is known about the possibility of cryptic female choice ( Eberhard 1996). Socha (2008) demonstrated that the sexual attractiveness of P. apterus males is correlated with their fertility, and both are probably related to the size of their accessory glands.

For the males in general it is very likely that their offspring number is strongly dependent on the females accessible to them, which is of course dependent on their sexual attractiveness. However, sometimes males can have a surplus of available females: this is the case if the sex ratio is strongly female biased or (a common case among insects!) a male is physiologically capable of only a limited, low number of copulations. In this case, it is advantageous for the males to choose the most fertile females available to them, and again, sexual attractiveness represents a clear reproductive advantage.

To the author’s knowledge, no empirical data has been published on the relationship between sexual attractiveness and offspring number of any blissid species, including I. sabuleti .

(c) Wing-mutilated macropters of I. sabuleti can be quite easily misidentified as brachypters to the superficial human observer. However, humans rely solely on visual cues for distinguishing the two morphs, and this is almost certainly not the case for the bugs assessing their potential sexual partners. At the present state of knowledge there is no evidence that the bugs can even tell the difference between the genuine macropters and brachypters. In the best-known case of the red firebug (see above), it is more probable that both females and males assess their potential sexual partners using olfactory or behavioural cues which are somewhat correlated with the wing form, rather than observing the wing form directly at all.

This might be the case as well for I. sabuleti , and if so, the ‘plastic surgery’ hypothesis should be rejected. However, the large surface of the exposed abdominal tergites of the brachypters might serve as a tactile and/or olfactory and/or visual key stimulus, which might render both brachypters and de-alated macropters sexually more attractive than the full-winged macropters, where the membrane almost entirely covers the abdomen. In the closely related Ischnodemus caspius Jakovlev, 1871 , the cuticular structures of the abdomen have been studied in detail by scanning electron microscopy ( Xue and Bu 2007). The abdominal scent gland is non-functional in the adults, and – as is general in the Blissidae family – there are pairs of so called ‘cell areas’ on the abdominal tergites. The function of these small, round, hairless spots showing a cell-like cuticular structure is unknown. They contain no visible pores, so they are unlikely to be pheromone glands, but perhaps might contain mechano- and/or chemoreceptors.

Vibrational communication of insects, including heteropterans, that produce no audible voice has received increasing attention in the last several decades ( Cokl and Virant-Doberlet 2003; Davranoglu et al. 2023). Unlike in some other heteropteran families, stridulatory (Aschlock et al. 1963) or tymbal ( Minghetti et al. 2020) organs are rather exceptional in Blissidae and not known in I. sabuleti . However, surface-transmitted vibratory communication by tremulation is possible even in the absence of any specialised sound-producing organ, as is described in P. apterus ( Benediktov 2007) . It is unknown whether I. sabuleti uses surface-transmitted vibratory signals during the courtship or in any other context; however, if it does, the character of the signal might be affected by the length of the hemielytra, and the signals of wing-mutilated macropters would probably resemble those of the brachypters. These considerations may apply also for wing-mutilating gerroids, as the water surface is a very efficient medium for vibrational communication.

Courtship behaviour of I. sabuleti must be studied in much more detail; however, according to the author’s sporadic observations, males mounting the females often vigorously rub the top of their abdomens against the distal part of the female’s body, which is covered with the membrane on the full-winged macropters while it is free on both genuine brachypters and de-alated macropters. Even if this is not a vibrational signal (see above), then it is still possible that the males find the touch of the naked tergites more attractive, or that the females become more receptive when they receive the stimulus of the male abdomen directly on their free tergites instead of on their membrane. In this case, both genuine brachypterous and de-alated macropterous females might be engaged more often in copulation than full-winged macropterous females. In this case it is even less clear how the females would observe the wing status of their potential partners. The potential role of visual and vibrational cues and of the tactile and/or olfactory examination of the partner with the antennas should be studied in detail.

In conclusion, the author suggests that the ‘plastic surgery hypothesis’ is interesting enough to be tested empirically, although the simpler alternative hypotheses presented above might have greater probability.

Figures

Figure 4. Seasonal change in the percentage of broken-winged male and female macropters at Darány in 2021. Numbers on the tops of the columns indicate the number of individuals examined. (All samples also contained a considerable percentage of brachypters which are not included in the figures).

Figure 5. Seasonal change in the percentage of broken-winged male and female macropters at Baranyahidvég in 2022. Numbers on the tops of the columns indicate the number of individuals examined. (All samples also contained a considerable percentage of brachypters which are not included in the figures).

Figure 6. Seasonal change in the percentage of broken-winged male and female macropters at Csörötnek in 20222. Numbers on the tops of the columns indicate the number of individuals examined. (All samples also contained a considerable percentage of brachypters which are not included in the figures).

Figure 7. Seasonal distribution of the full-winged and broken-winged macropters in the collection of the Hungarian Natural History Museum.