Ischnodemus sabuleti

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 orboth? 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 anapomorphic, evolutionary ‘primitive’ phenomeno