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Pupal Traits and Adult Emergence in the Pine Processionary Moth Thaumetopoea Pityocampa (Lepidoptera: Notodontidae) Are Affected by Pupal Density

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Pupal Traits and Adult Emergence in the Pine Processionary Moth Thaumetopoea Pityocampa (Lepidoptera: Notodontidae) Are Affected by Pupal Density EUROPEAN JOURNAL OF ENTOMOLOGYENTOMOLOGY ISSN (online): 1802-8829 Eur. J. Entomol. 116: 320–329, 2019 http://www.eje.cz doi: 10.14411/eje.2019.035 ORIGINAL ARTICLE Pupal traits and adult emergence in the pine processionary moth Thaumetopoea pityocampa (Lepidoptera: Notodontidae) are affected by pupal density CARMELO P. BONSIGNORE 1, FRANCESCO MANTI 1, ELVIRA CASTIGLIONE 1 and ANDREA BATTISTI 2 1 Laboratorio di Entomologia ed Ecologia Applicata – Dipartimento PAU, Università degli Studi Mediterranea di Reggio Calabria, Reggio Calabria, Salita Melissari s.n, 89100, Italy; e-mails: [email protected], [email protected], [email protected] 2 DAFNAE, University of Padova, Agripolis, 35020 Legnaro, Italy; e-mail: [email protected] Key words. Lepidoptera, Notodontidae, Thaumetopoea pityocampa, cocoon, gregariousness, pupal density, pupal size, emergence, Pinus Abstract. The expectation is that the phenology of an herbivore is infl uenced by abiotic factors and its own population density dur- ing development. In this study, we investigated how the pupal density affected the pupal traits and emergence of Thaumetopoea pityocampa moths over a period of 3 years in two clearings in a pine forest. The pupae were larger in years when the pupal density was high and in the clearing exposed to less solar radiation. There was no relationship between the time of pupation and pupal size. Large pupae were positively correlated with an early emergence of adult moths and a longer period of adult emergence. Up to 13.9% of the pupae developed without cocoons, especially in years when they were abundant, but this did not affect the emer- gence of the moths. Incidence of pupal diapause was density-dependent and only occurred at a low level in dense populations. Overall, our results indicate that gregariousness confers important fi tness-related advantages in this species. INTRODUCTION spin a silken cocoon in which they pupate. The duration of In some Lepidoptera, such as the pine processionary the period from larval emergence to pupation varies from moth (PPM; Thaumetopoea pityocampa [Denis & Schif- year to year and site to site, and the total period may be up fermüller, 1775]), the pupae develop in the soil close to to 2 months (Demolin, 1971; Buxton, 1990; Bonsignore the trees that were inhabited by the larvae. The PPM is a et al., 2015; Robinet et al., 2015). The larvae select sites univoltine species and is widespread in the Mediterranean, well exposed to sun, e.g., the edge of a forest, where the including southwest Europe, the Balkans and North Africa thermal conditions and/or the microclimatic conditions in (Roques, 2015). This species is one of the most important the soil are favourable (Dulaurent-Mercadal et al., 2011; pests of various types of pines and cedars, and can hin- Samalens & Rossi, 2011). The habitat infl uences pupation der the growth of infested trees (Jacquet et al., 2012). The success and survival in PPMs (Markalas, 1989; Dulaurent- spread of this pest into new areas requires the presence of Mercadal et al., 2011; Torres-Muros et al., 2017), and the appropriate host plants and is facilitated by climate warm- pupae suffer additional mortality due to natural enemies, ing or a high population density (Hodar & Zamora, 2004; such as parasitoids (Bonsignore et al., 2015), predacious Battisti et al., 2005; Castagneyrol et al., 2016). birds (Barbaro & Battisti, 2011) and entomopathogenic Pine processionary moth lays its eggs on pine needles fungi (Er et al., 2007). The adults emerge during summer, during summer. The eggs hatch 30 to 45 days later (Aydın but some pupae can spend 2 or more years in diapause and et al., 2018). Thus, the larvae feed throughout autumn and the adults generally disperse over short distances (Bon- during winter and spring depending on temperature. The signore & Manti, 2013; Roques, 2015). larvae are gregarious from early on in their development Pupation has a physiological basis as it is associated with and spin conspicuous tents in tree tops. After completing reaching a particular size (D’Amico et al., 2001; David- their feeding, generally during late winter, larvae typical- owitz et al., 2003). Traits such as pupal weight or size are ly form a procession in which they walk head to tail in a considered important because they can affect the longevity column to reach their pupation sites on the ground. They of females and fi tness of adults (Calvo & Molina, 2005; then burrow into the soil to a depth of a few centimeters, Fantinou et al., 2008). For example, pupal size may affect Final formatted article © Institute of Entomology, Biology Centre, Czech Academy of Sciences, České Budějovice. An Open Access article distributed under the Creative Commons (CC-BY) license (http://creativecommons.org/licenses/by/4.0/). 320 Bonsignore et al., Eur. J. Entomol. 116: 320–329, 2019 doi: 10.14411/eje.2019.035 male phenotype, which could infl uence male mating suc- of pupae in each clearing) in order to obtain a better un- cess (Fox et al., 1995). The relationships between pupal derstanding of development during the pupal stage and its traits and pupal density in gregarious Lepidoptera may effect on the adult phenology of PPM. vary according to the population dynamics of a species and are not easy to understand. Pine processionary moth MATERIALS AND METHODS infestations are not evenly distributed within pine forests Experimental site and mainly occur at the edges of pine stands (Samalens & Two pupation areas located in two clearings in a Pinus nigra Rossi, 2011). Several studies have shown that the adults forest in Aspromonte National Park, Calabria (South Italy) are more likely to oviposit near the edges of pine stands (38°04´10˝N and 15°49´38˝E, at 1200 m above sea level) were (Samalens & Rossi, 2011) than more than 25 m from the studied for three years (2010–2012). The vegetation in both edges (Parlak et al., 2019). Thus, clearings within forests clearings (designated as A and B) consisted of grassland and low 2 are suitable sites for PPMs as they create edges and open shrubs. Area A (ca 175 m ) had a south-easterly aspect and a slope of 5%. Area B (about 403 m2) had a south-westerly aspect and a areas where their processioning larvae can pupate in sun- slope of 4%. The distance between the two sites was about 70 exposed soils. Pine forests with suitable pupation sites for m and they were also separated by a dirt road between the pine supporting large aggregations of PPM occur in southern trees, which limited the movement of larvae between the two Italy (Bonsignore et al., 2011, 2015). areas (Fig. 1). The soil in areas A and B did not differ in terms of The relationships between pupal traits, population den- pH (5.8–6.0) and texture (sand 88%, silt 5–9%, clay 3–7% and sity and adult phenology in PPM need to be determined in total limestone 1%) and the average organic matter content in the order to better understand the mechanisms that determine top 15-cm layer was 22.4–26.4%. the relationships between their development and environ- The temperatures during the period of the study were obtained mental variables. Over a period of 3 years we investigated from a weather station (ARPACAL, Regional Agency for Envi- ronmental Protection of Calabria) located close to the sites stud- two clearings within a pine forest where pupae developed. ied (see Supplementary Fig. S1). Microclimatic differences be- We studied PPM from when the larvae pupated in the soil tween the two areas, including solar radiation, temperature and until the moths emerged. We aimed to determine whether soil moisture, were recorded for one season (from April 1 to July pupal traits such as size and presence or absence of a co- 30, 2014, while pupae were in the soil) at an interval of 15-min coon varied in time and with population density (number at a height of 1.80 m above the ground and 10 cm deep in the Fig. 1. Map showing the geographical locations of areas A and B in which the marked colonies pupated. Circles of different colours in boxes indicate the fl ags used for identifying the different pupal colonies. 321 Bonsignore et al., Eur. J. Entomol. 116: 320–329, 2019 doi: 10.14411/eje.2019.035 soil using Micro Station HOBO® data loggers (Onset Computer mean pupa length was analyzed using Spearman’s correlation co- Corporation, Bourne, USA). The assessment of solar radiation effi cient. Pupal length and weight were analyzed independently showed that area A was less exposed than area B. The average using ANOVA. The factors included in the full factorial model solar radiation (day and night) (W/m2) for area A was 72.69 and included the year and clearing. Linear regression was used to de- that for area B was 193.30. Area A was cooler and moister than termine the relationship between the mean pupal length and the area B, with an average temperature of 13.95°C for area A and total number of individuals that pupated on each date. 14.57°C for area B (see Supplementary Fig. S2) and the soil The percentage of pupae without cocoons was calculated for moisture (volume of water per volume of soil, m³/m³) in the fi rst each year and compared with the density of individuals at each 10 cm was 0.1529 for area A and 0.062 for area B. pupation site. For all years, the percentages were compared using a chi-squared (χ2) test of the equality of distributions. The weights Survey of pupation sites and pupae collection of the cocoons in different years were compared using ANOVA.
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