Chorology, flight curves and diel activity of oak-living clear-wing moths in Extremadura, SW Spain (Lepidoptera: Sesiidae)

Introduction

The sesids or clear-wing moths (Lepidoptera: Sesiidae) are a striking family of diurnal and heliophilous moths whose adults exhibit a marked Batesian mimicry with the Hymenoptera, both in their appearance (aposematic coloration often with yellow or red rings in the abdominal segments, partly transparent wings with scaleless areas) and in their behaviour (hovering flight). Adults of many species have functional mouthparts and visit flowers during the daytime to feed on, although the exact diel period of activity is often species-specific and weather-sensitive. The larvae of sesids are phytophagous and endophagous, with little pigmentation, usually with cream-white urites and a brown head/prothoracic shield (Laštůvka & Laštůvka, 2001Laštůvka Z, Laštůvka A, 2001. The Sesiidae of Europe. Apollo Books, Stenstrup. 245 pp.
).

Several clear-wing moths have specialised in woody host plants (xylophagous species), often of closely related hosts (oligophagous species). Larvae of these sesid species bore into the wood of the trunk, branches and/or roots of their host trees and shrubs during larval development (1-4 years). Xylophagous sesids require living wood for their development, even if some species prefer damaged, decayed, or diseased hosts (Pühringer, 1994Pühringer F, 1994. Zur Biologie der oberösterreichischen Glasflügler (Lepidoptera, Sesiidae). Entomol Arbeits Salzkammergut 1: 1–84.
). Larvae develop under the host bark, boring irregular galleries in the cambium zone and at the interface between dead and living tissues. Larval galleries may be more or less grouped, even merged, with abundant silk and reddish-brown frass that may be expelled to the outside. Larval galleries are often associated with bark wounds and cracks, thickened edges around debarked areas, bark previously altered by mistletoe plants and other epiphytes, excrescences, tumescence, fungal swellings, and bacterial cankers (Audemard & Vigouroux, 1982Audemard H, Vigouroux A, 1982. Une curieuse association parasitaire sur Pêcher, Sésie et tumeur bactérienne du collet. Phytoma Def Veg 337: 28–29.
; Pühringer, 1994Pühringer F, 1994. Zur Biologie der oberösterreichischen Glasflügler (Lepidoptera, Sesiidae). Entomol Arbeits Salzkammergut 1: 1–84.
). Xylophagous sesids can cause significant damage to their host plants (Fig. 1), so that some species are considered important pests of fruit and forest trees and shrubs (Allen, 1975Allen AA, 1975. Notes on a colony of Synanthedon vespiformis L. (Yellow-legged clearwing) in S.E. London (N.W. Kent) with special reference to the breeding site. Entomol Rec J Var 87: 47–49.
; Laštůvka & Laštůvka, 2001Laštůvka Z, Laštůvka A, 2001. The Sesiidae of Europe. Apollo Books, Stenstrup. 245 pp.
).

In recent years, damage by sesids to fagaceous trees has been reported in different areas of Extremadura (SW Spain), specifically Synanthedon vespiformis (L.) in young chestnut plantations (Armendáriz et al., 2014Armendáriz J, Aza C, Bañuls P, Manzano M, Mateos J, 2014. Synanthedon vespiformis, un problema emergente en los castañares del norte de Cáceres. Phytoma España 255: 31–35.
) and in reforestations done in oak open woodlands (Del Moral et al., 2013Del Moral J, Casadomet E, Rebollo FJ, Moral FJ, Trigo E, Villafaina M, Villalba JA, 2013. Distribución de los daños de Synanthedon vespiformis en reforestaciones de encinas y alcornoques de la provincia de Badajoz. I Congreso de la Dehesa y el Montado, Badajoz (España), November 6–7, 2013.
), although in many other cases the species membership of the sesids causing damage was unknown. Evidence of the poor knowledge of the clear-wing moths in the study region arises from the preliminary results of this study, which has provided the first provincial records of some sesid species associated with oaks (Montero-Calvo & Blázquez-Caselles, 2023Montero-Calvo AJ, Blázquez-Caselles A, 2023. Sesiidae en Extremadura (España): Revisión y nuevas citas (Insecta: Lepidoptera). Arquiv Entomol 26: 155–168.
; Torres-Vila & Montero-Calvo, 2024Torres-Vila LM, Montero-Calvo A, 2024. Adenda a los sésidos (Lepidoptera: Sesiidae) de Extremadura (SO España). Arquiv Entomol 28: 137–140.
). Although sesid damage may occur in oaks of any age, the most severe impact often occurs in young plants because the subcortical larval galleries can gird and kill the host. Girdling can occur quickly with crowded larval populations, but also due to damage accumulated over years. Damage from sesids is widespread in oak reforestations and densifications, where larvae can cause substantial mortality in young trees in the first years after plantation. The objective of this study was to determine the clear-wing moth species associated with oaks in the region of Extremadura, as well as acquire knowledge on their chorology, flight curves and diel activity.

Material and methods

Results

Chorology

 ⌅

Four of the six target species, P. insolita, S. vespiformis, S. codeti and S. conopiformis were well distributed throughout the study region, occurring in the three sampled forest habitats (holm, cork, and Pyrenean oak) and occupying a considerable altitudinal range (Fig. 2, Suppl. Table S1). On the contrary, S. stomoxiformis and S. spuleri were never captured. The total number of catches per species, as well as the species-specific values of abundance and occupancy, differed noticeably among species (Fig. 4). S. conopiformis was the most abundant species, but the moth with the highest occupancy was P. insolita, despite its relatively low abundance (Fig. 4). Note, however, that S. vespiformis autumn flight (see below) is not included in these statistics since trapping protocol only covered the spring (April-June). It follows that S. vespiformis abundance values are underestimated if the entire year is considered rather than just the spring period.

Figure 2.  Chorology of the four species of oak-living clear-wing moths detected in Extremadura (SW Spain) (n = 37 sites, see Suppl. Table S1) using pheromone traps: Paranthrene insolita, Synanthedon conopiformis, Synanthedon codeti and Synanthedon vespiformis. The 10 × 10 km UTM grid (datum ETRS89) is superimposed on the map.

Figure 3.  Automated traps used in this study to assess the diel activity of the target clear-wing moth species in the wild. A: a phototrap set in a Pyrenean oak forest (Montánchez, Cáceres, April 20, 2023; site/year code: 46F); B: detail of the phototrap; C: an infrared-sensor trap set in a cork oak open woodland (Santibáñez el Bajo, Cáceres, April 19, 2021; site/year code: 22S); D: detail of the infrared-sensor trap (opened) showing the arrangement of the electronic components. See text for a detailed description.

Figure 4.  Total number of catches during this study (A), abundance (B), and occupancy (C) of the clear-wing moth species captured in the pheromone traps: four oak-living target species (green bars): Paranthrene insolita (Pins), Synanthedon conopiformis (Scon), Synanthedon codeti (Scod) and Synanthedon vespiformis (Sves); and three main non-target sesid species (red bars): Bembecia uroceriformis (Buro), Pyropteron chrysidiformis (Pchr) and Pyropteron leucomelaena (Pleu). Vertical lines (panel B) represent the standard error of the mean. See text for a definition of the abundance and occupancy variables.

The commercial sex pheromones used showed a good level of specificity. Even so, there was cross-attraction with three non-target sesids (not associated with oaks) that were captured in the traps (Suppl. Table S1, Fig. 4), in order of abundance: Bembecia uroceriformis (Treitschke, 1834), Pyropteron chrysidiformis (Esper, 1782) and Pyropteron (Synansphecia) leucomelaena (Zeller, 1847). The occupancy of these three non-target species did not exceed 20% in any case (Fig. 4). It is important to note that the S. conopiformis sex pheromone was extremely attractive to B. uroceriformis; in fact, all B. uroceriformis specimens were captured in traps baited with S. conopiformis pheromone (see Pühringer, 1996Pühringer F, 1996. Utilities zum Pheromonfang von Sesien (Lepidoptera, Sesiidae). Entomol Nachr 3: 8–12.
).

Flight curves

 ⌅

The flight curves showed that P. insolita (Fig. 5A) and S. conopiformis (Fig. 5B) exhibit spring activity (April-June), with flight peak dates that may vary up to almost a month depending on the site and year. The data available for S. codeti were more modest but clearly indicate that its flight period is longer and later (May-October) than in the two preceding species, with a marked summer peak (July) (Fig. 5C). In the case of S. vespiformis, adult activity covered the longest seasonal period (early April to early November), with two flight peaks in May and September-October (Fig. 5D).

Figure 5.  Flight curves (average weekly catches per trap) of four target species of clear-wing moths: Paranthrene insolita (A), Synanthedon conopiformis (B), Synanthedon codeti (C), and Synanthedon vespiformis (D), obtained in various sites and years in Extremadura (see Suppl. Table S1 for a key to the site/year codes given in square brackets).

Moth size in S. vespiformis was not normally distributed (Shapiro-Wilk test, W = 0.98, P < 0.01). Moth size was significantly affected by the season (Analysis of deviance, LR Chi² = 16.61, df = 2, P < 0.001) but not by the year (LR Chi² = 0.51, df = 1, P = 0.48), with no season × year interaction (LR Chi² = 0.06, df = 2, P = 0.97) (Fig. 6). So, we pooled both years and re-analysed the data with the season as the only explanatory variable (LR Chi² = 16.40, df = 2, P < 0.001). A post hoc of this model showed that S. vespiformis moths were significantly larger in spring than in either summer (|z| = 3.73, P < 0.001) or autumn (|z| = 3.01, P < 0.01), with no significant differences between the summer and autumn seasons (|z| = 0.05, P = 0.99) (Fig. 6).

Figure 6.  Mean adult size (forewing length, mm) of Synanthedon vespiformis males caught in pheromone traps for two consecutive years (2022-2023), depending on the season (spring, summer and autumn). Means labelled with different lowercase letters (pooled years) are significantly different (P < 0.01). Vertical lines represent the standard error of the mean. See text for a full statistical analysis.

Diel activity

 ⌅

Diel activity was notably different between the three target species for which data were available: P. insolita, S. vespiformis and S. conopiformis (Fig. 7). Although the three species were active from early afternoon until late evening (from about 14:00 to 22:30 h), the earliest flight peak was that of P. insolita (15:00-18:00 h), followed by S. vespiformis (17:00-19:00 h), and then by S. conopiformis (19:00-21:00 h) (Fig. 7). Diel activity was significantly earlier in S. vespiformis than in S. conopiformis (KS test, D-stat = 0.642 > D-crit = 0.110, P < 0.001). KS tests were not computed with P. insolita due to the low sample size recorded for this species in automated traps. Distinctly enough, the diel activity of B. uroceriformis (a non-target sesid species) took place in the morning, with a relatively early flight peak (9:00-11:00 h) (Fig. 7) (all local time, GMT+2).

Figure 7.  Diel activity (hourly flight frequency, %) in Extremadura of three target species of clear-wing moths: Paranthrene insolita, Synanthedon conopiformis and Synanthedon vespiformis; and one non-target sesid species: Bembecia uroceriformis, as assessed with automated traps in two sites for three years (site/year codes: 22S, 43S, 44F and 46F; see Suppl. Table S1; data pooled within species).

Discussion

Abundance and occupancy values show overall that the most frequent sesid species associated with oaks in Extremadura are S. conopiformis and S. vespiformis, followed at some distance by P. insolita and S. codeti, although in the case of the last species, more information would be useful to better ascertain its actual impact on oaks. The presence of S. stomoxiformis was not detected despite having been reported from relatively close Spanish provinces and Portuguese districts (Laštůvka & Laštůvka, 2014Laštůvka Z, Laštůvka A, 2014. Sesiidae of the Iberian Peninsula, new records and distributional analysis (Insecta: Lepidoptera). SHILAP Rev Lepid 42: 559–580.
; Álvarez et al., 2021Álvarez M, Aguado LO, Noval N, Álvarez P, 2021. New data, updated distributions and flower preferences of the clearwing moths (Lepidoptera, Cossoidea, Sesiidae) of mainland Spain. Bol SEA 68: 289–305.
), possibly due to the more xeric conditions of most sampled habitats in Extremadura. The non-detection of S. spuleri was not surprising since this species is only known in Spain from the province of Lleida (Álvarez et al., 2021Álvarez M, Aguado LO, Noval N, Álvarez P, 2021. New data, updated distributions and flower preferences of the clearwing moths (Lepidoptera, Cossoidea, Sesiidae) of mainland Spain. Bol SEA 68: 289–305.
). Our occupancy estimates must be considered quite robust (including particularly absence data) because it is highly unlikely that a pheromone trap fails to detect a local population over a full flight season, considering the high levels of detectability that sexual pheromones provide, specifically in clear-wing moths (Burman et al., 2016Burman J, Westerberg L, Ostrow S, Ryrholm N, Bergman KO, Winde I, Nyabuga FN, Larsson M, Milberg P, 2016. Revealing hidden species distribution with pheromones: the case of Synanthedon vespiformis (Lepidoptera: Sesiidae) in Sweden. J Insect Conserv 20: 11–21. http://dx.doi.org/10.1007/s10841-015-9835-9
).

Automated trap data showed that the diel activity of the three species studied may extend from early afternoon to late evening, but flight peaks were clearly different between species, first P. insolita, then S. vespiformis and finally S. conopiformis, which reveals that each species displays a preferred diel flight period. Activity times were quite similar to those reported in central Europe, despite the latitude difference (Pühringer, 1994Pühringer F, 1994. Zur Biologie der oberösterreichischen Glasflügler (Lepidoptera, Sesiidae). Entomol Arbeits Salzkammergut 1: 1–84.
, 1996Pühringer F, 1996. Utilities zum Pheromonfang von Sesien (Lepidoptera, Sesiidae). Entomol Nachr 3: 8–12.
; Szántóné-Veszelka et al., 2010Szántóné-Veszelka M, Poós B, Szőcs G, 2010. Blackberry and raspberry, new hosts of the yellow legged clear-wing moth, Synanthedon vespiformis: what can the recently developed sex attractant offer in monitoring and beyond? IOBC Working Group, Integrated Plant Protection in Fruit Crops Subgroup “Soft Fruits”, 7th Workshop on Integrated Soft Fruit Production, pp: 20–23.
). In the case of P. insolita, diel activity was similar to that reported in Turkey and other Spanish regions, irrespective of the subspecies considered (Spatenka & Laštůvka, 1997Spatenka K, Laštůvka Z, 1997. Zur Verbreitung und Variabilität von Paranthrene insolita Le Cerf, 1914 (Lepidoptera, Sesiidae). Nachr Entomol Ver Apollo NF 18: 13–21.
).

Seasonal flight curves were considerably different between species. Adult activity of P. insolita and S. conopiformis was in spring, that of S. codeti was in summer, and distinctly S. vespiformis activity extended over a long period from spring to autumn, as previously reported (Levi-Zada et al., 2011Levi-Zada A, Ben-Yehuda S, Dunkelblum E, Gindin G, Fefer D, Protasov A, Kuznetsowa T, Manulis-Sasson S, Mendel Z, 2011. Identification and field bioassays of the sex pheromone of the yellow-legged clearwing Synanthedon vespiformis (Lepidoptera: Sesiidae). Chemoecology 21: 227–233. http://dx.doi.org/10.1007/s00049-011-0081-7
; Armendáriz et al., 2014Armendáriz J, Aza C, Bañuls P, Manzano M, Mateos J, 2014. Synanthedon vespiformis, un problema emergente en los castañares del norte de Cáceres. Phytoma España 255: 31–35.
). However, flight curves recorded in Extremadura differed ostensibly from the phenology reported in the Pühringer’s (2024)Pühringer F, 2024. Phenology of Palearctic clear wing moths (Lepidoptera: Sesiidae). https://www.sesiidae.net/phenology.htm [2 May 2024].
database: in Extremadura, P. insolita and S. conopiformis showed earlier activity (roughly a month); S. codeti showed later activity (about a month), while S. vespiformis showed a much longer activity period, especially at the end of the season (from early April to mid-November).

The case of S. vespiformis deserves special attention. Captures as late as those observed in this study (until mid-November) had never been reported before to our knowledge. Furthermore, flight curves in Montánchez showed for two years a marked bimodal pattern, with well-differentiated maxima in spring and autumn and minimal (or non-existent) moth population during the summer. In other sites/years, the bimodal pattern of S. vespiformis was less evident, likely due to a lower number of trap catches. A bimodal flight pattern, although less pronounced, has also been reported in Extremadura in a previous study (Armendáriz et al., 2014Armendáriz J, Aza C, Bañuls P, Manzano M, Mateos J, 2014. Synanthedon vespiformis, un problema emergente en los castañares del norte de Cáceres. Phytoma España 255: 31–35.
). Further field research is needed to determine whether the bimodal flight pattern of S. vespiformis reported here is widespread in southern Iberia or just occurs locally due to unknown ecological and meteorological factors. In any case, the bimodal flight pattern does not fit with the presence data reported in central European countries, where S. vespiformis either displays a more-or-less continuous flight through the season (Szántóné-Veszelka et al., 2010Szántóné-Veszelka M, Poós B, Szőcs G, 2010. Blackberry and raspberry, new hosts of the yellow legged clear-wing moth, Synanthedon vespiformis: what can the recently developed sex attractant offer in monitoring and beyond? IOBC Working Group, Integrated Plant Protection in Fruit Crops Subgroup “Soft Fruits”, 7th Workshop on Integrated Soft Fruit Production, pp: 20–23.
; Schmitt et al., 2021Schmitt J, Bartsch D, Markl G, 2021. Verbreitung, Habitatnutzung und Phänologie der Glasflügler im Raum Tübingen (Lepidoptera: Sesiidae). Carolinea 79: 83–112. https://doi.org/10.57962/regionalia-20315
) or maximum catches in June-July (Pühringer, 2024Pühringer F, 2024. Phenology of Palearctic clear wing moths (Lepidoptera: Sesiidae). https://www.sesiidae.net/phenology.htm [2 May 2024].
), precisely when moth populations are low or absent in our study area.

The bimodal flight pattern of S. vespiformis detected in Extremadura should not be mistakenly interpreted as a bivoltine one, i.e., the result of two annual larval generations. Although it has been suggested that S. vespiformis may have more than one generation (Armendáriz et al., 2014Armendáriz J, Aza C, Bañuls P, Manzano M, Mateos J, 2014. Synanthedon vespiformis, un problema emergente en los castañares del norte de Cáceres. Phytoma España 255: 31–35.
), the occurrence of two or more generations per year has never been proven in a xylophagous sesid species to our knowledge. Woodborers in general, and sesids in particular, show a rather slow development due to the low nutritional quality of the wood. So, it is unlikely that in just about six months (May-October) the offspring of spring adults will complete their life cycle to produce the autumn flight (see Pühringer, 1994Pühringer F, 1994. Zur Biologie der oberösterreichischen Glasflügler (Lepidoptera, Sesiidae). Entomol Arbeits Salzkammergut 1: 1–84.
). Whether autumn adults were the progeny of spring adults, this would also imply that S. vespiformis does not exhibit obligate diapause. Even less likely would be that the offspring of the autumn flight could complete their development under winter cold conditions to emerge in the next spring. Moreover, S. vespiformis larvae likely stop their development and overwinter. Finally, the fresh appearance and absence of desquamation of the adults captured in early autumn suggest their recent emergence from the pupa, which would rule out that they are spring adults experiencing aestivation.

The bimodal flight distribution of S. vespiformis is likely to be the result of a single generation, but with two well-differentiated periods of adult emergence. It has been suggested that spring rainfall (early March) and summer storms (late July-early August) could be used as cues by S. vespiformis to initiate the spring and autumn emergence periods, respectively (Crégu, 2019Crégu A, 2019. Ecologie et chorologie d’une famille de lépidoptères méconnue, les Sesiidae. Mémoire Diplôme de l’École Pratique des Hautes Études, MNHN-PSL Research University, Paris. 107 pp.
). On the contrary, it has also been speculated that bimodal flight could result from low flight activity in the early summer rainy period (Schmitt et al., 2021Schmitt J, Bartsch D, Markl G, 2021. Verbreitung, Habitatnutzung und Phänologie der Glasflügler im Raum Tübingen (Lepidoptera: Sesiidae). Carolinea 79: 83–112. https://doi.org/10.57962/regionalia-20315
). In any case, available evidence suggests that a part of the S. vespiformis population uses the strategy of flying in spring and the rest in autumn. The bimodal pattern could be adaptive if it evolves to avoid extreme summer conditions of heat and drought, which are increasingly frequent in SW Spain under the current climate change scenario. The smaller body sizes of summer and autumn adults than spring adults agree with this idea, since it suggests that the larvae of both groups have endured different thermal conditions during their development. The smaller size of the summer and autumn adults could derive from the fact that larvae completed the final stages of development in the hot season, as larval growth speed in insects increases with temperature at the cost of producing smaller adults (Torres-Vila, 1996Torres-Vila LM, 1996. Efecto de la temperatura de desarrollo preimaginal sobre el potencial biótico de la polilla del racimo de la vid, Lobesia botrana (Denis y Schiffermüller, [1775]) (Lepidoptera: Tortricidae). SHILAP Rev Lepid 24: 197–206.
; Angilletta et al., 2004Angilletta MJ, Steury TD, Sears MW, 2004. Temperature, growth rate, and body size in ectotherms: fitting pieces of a life-history puzzle. Integr Comp, Biol 44: 498–509. http://dx.doi.org/10.1093/icb/44.6.498
; Kingsolver & Huey, 2008Kingsolver J, Huey R, 2008. Size, temperature, and fitness: three rules. Evol Ecol Res 10: 251–268.
). Tree physiology-mediated seasonal differences in the quality of food available to larvae could also be involved in the adult size variation observed. Consistent with these ideas, small and large S. vespiformis larvae can be found at the same time in the same host, although they can reach adulthood the same year (FES, 2024FES [Flemish Entomological Society], 2024. Catalogue of the Lepidoptera of Belgium, Synanthedon vespiformis (Linnaeus, 1761). https://projects.biodiversity.be/lepidoptera/species/4920/ [24 April 2024].
).

The bimodal flight pattern of S. vespiformis also poses an interesting ecological and evolutionary scenario. In the absence of gene flow between the spring and autumn moth phenotypes, life-history theory predicts that the temporal segregation of both phenotypes should promote a speciation process. Drivers that could act against speciation by allowing gene flow between both seasonal phenotypes are the few summer adults (serving as a “bridge” between spring and autumn) and the larval development of more than a year in a fraction of the population (FES, 2024FES [Flemish Entomological Society], 2024. Catalogue of the Lepidoptera of Belgium, Synanthedon vespiformis (Linnaeus, 1761). https://projects.biodiversity.be/lepidoptera/species/4920/ [24 April 2024].
) whose emergence period could putatively occur in spring or summer. It follows that the life cycle of S. vespiformis in SW Iberia deserves additional study.

In conclusion, our research contributes to a better knowledge of the chorology, phenology, ecology and behaviour of the main clear-wing moth species associated with oaks in SW Spain, P. insolita, S. conopiformis, S. codeti and S. vespiformis. This information will be useful to improve integrated pest management methods given the increasing phytosanitary impact of these woodborers on oak open forests in Extremadura and other Iberian regions.

Supplementary material

(Table S1) accompanies the paper on Forest Systems’ website.

Data availability

Additional data beyond those already provided in this paper will be made available on reasonable request to the first author.

Competing interests

The authors have declared that no competing interests exist.

Authors’ contributions

Luis M. Torres-Vila: Conceptualization, Formal analysis, Investigation, Methodology, Resources, Supervision, Writing - original draft, Writing - review & editing. Adrián J. Montero-Calvo: Conceptualization, Investigation, Methodology, Resources, Software, Supervision, Writing - review & editing. Javier Mendiola-Díaz: Investigation, Methodology, Writing - review & editing. Rafael López-Calvo: Conceptualization, Investigation, Methodology, Software, Writing - review & editing. Álvaro Sánchez-González: Investigation, Methodology, Writing - review & editing. Francisco Ponce-Escudero: Investigation, Methodology, Writing - review & editing. Félix Fernández-Moreno: Investigation, Methodology. Zdeněk Laštůvka: Conceptualization, Investigation, Methodology, Writing - review & editing.

Funding

References