EN62CH18-Battisti ARI 22 December 2016 11:31 ANNUAL REVIEWS Further Click here to view this article's online features: • Download figures as PPT slides • Navigate linked references • Download citations Processionary Moths and • Explore related articles • Search keywords Associated Urtication Risk: Global Change–Driven Effects Andrea Battisti,1,∗ Stig Larsson,2 and Alain Roques3 1Department DAFNAE, University of Padova, Legnaro I-35020, Italy; email: [email protected] 2Department of Ecology, Swedish University of Agricultural Sciences, Uppsala S-75007, Sweden; email: [email protected] 3Forest Zoology, UR INRA 0633, Orleans´ F-45075, France; email: [email protected] Annu. Rev. Entomol. 2017. 62:323–42 Keywords First published online as a Review in Advance on climate, health, Notodontidae, plant trade, seta, Thaumetopoeinae November 16, 2016 The Annual Review of Entomology is online at Abstract ento.annualreviews.org Processionary moths carry urticating setae, which cause health problems This article’s doi: Annu. Rev. Entomol. 2017.62:323-342. Downloaded from www.annualreviews.org in humans and other warm-blooded animals. The pine processionary moth 10.1146/annurev-ento-031616-034918 Thaumetopoea pityocampa has responded to global change (climate warming Copyright c 2017 by Annual Reviews. and increased global trade) by extending its distribution range. The subfam- Access provided by Swedish University of Agricultural Sciences on 03/29/17. For personal use only. All rights reserved ily Thaumetopoeinae consists of approximately 100 species. An important ∗ Corresponding author question is whether other processionary moth species will similarly respond to these specific dimensions of global change and thus introduce health haz- ards into new areas. We describe, for the first time, how setae are distributed on different life stages (adult, larva) of major groups within the subfamily. Using the available data, we conclude that there is little evidence that pro- cessionary moths as a group will behave like T. pityocampa and expand their distributional range. The health problems caused by setae strongly relate to population density, which may, or may not, be connected to global change. 323 EN62CH18-Battisti ARI 22 December 2016 11:31 INTRODUCTION Processionary moths are members of the Notodontidae, which is known for carrying urticating Notodontidae: setae and thus causing health problems in humans and domesticated animals (8). Most of what family of Lepidoptera is known about these organisms and the health problems they cause comes predominately from including some 3,800 studies on one species, Thaumetopoea pityocampa. Here we broaden the perspective to include setae- species at the world related health issues for all the main clades within the Thaumetopoeinae; the subfamily includes level and occurring in all continents; mainly some 100 species (120). associated with trees T. pityocampa is frequently cited as an example of an insect favored by climate warming (9, 87, and shrubs 102) with improved winter survival resulting in recent expansion of the distribution range (11, Urticating setae: 100). An important question then is whether T. pityocampa can be considered a model species special type of hair for the processionary moths in general and thus whether health problems associated with other produced by the urticating species can similarly be expected to increase with climate warming. integument and Response to present and future climate change and the associated risks to human and domes- released by the insect for protection from ticated animal health have recently been reviewed for species within the genus Thaumetopoea in predators, causing Europe and the Mediterranean basin (108). However, this work did not consider the processionary reactions of external moths present in other continents that carry urticating setae. The morphology and function of and internal tissues urticating setae in arthropods, as well as their medical impact, have been reviewed but again with that lead to a variety of a similar focus on Thaumetopoea species (8). symptoms in humans and warm-blooded Here we review how major taxa within the Thaumetopoeinae vary with respect to urticating animals setae and, with this information, draw tentative conclusions about risks among taxa for instigating health problems in humans and domesticated animals. In addition, we assess whether these prob- lems can be expected to be more severe in a future characterized by increasing warming as well as global trade. DIVERSITY AND GLOBAL DISTRIBUTION OF PROCESSIONARY MOTHS The Thaumetopoeinae, the processionary moth subfamily, was formerly considered a self-standing family (Thaumetopoeidae) (62). However, it is now considered a homogeneous clade within Notodontidae, either basal according to the cladistic analysis of Miller (83) or well nested within this family based on molecular phylogeny (150) (Figure 1). The Thaumetopoeinae is composed of approximately 100 species in 20 genera occurring in Africa (including Madagascar), the Mediter- ranean, Europe, Asia, and Australasia in a belt from the Middle East to Taiwan, New Caledonia, and Australia (120). Annu. Rev. Entomol. 2017.62:323-342. Downloaded from www.annualreviews.org According to recent advances in morphological and molecular phylogenetic analyses of the group (6), three major clades can be identified (Figure 1). The first includes the Australian genera Epicoma and Ochrogaster and possibly seven other genera still unexplored, for a total Access provided by Swedish University of Agricultural Sciences on 03/29/17. For personal use only. of 30 known species. The second clade includes the African genera Anaphe, Epanaphe, Hyp- soides,andParadrallia and five other genera, for a total of 55 species. The third clade in- cludes the African, Asian, and European genera Gazalina and Thaumetopoea, for a total of 18 species. The European species of Thaumetopoea are by far the most studied and were reviewed first by Agenjo (2) and then by de Freina & Witt (30, 31), who split them into three genera (Helianthocampa, Thaumetopoea, Traumatocampa) using morphological traits of the adults. A molecular phylogeny of this group published in 2013 (123) strongly supports parallel evolution of the morphological traits used to divide Thaumetopoea into three distinct genera, suggesting that all species should be treated as members of a single genus, Thaumetopoea. 324 Battisti · Larsson · Roques EN62CH18-Battisti ARI 22 December 2016 11:31 Fabaceae Ochrogaster (2) Myrtaceae I Casuarinaceae (19) Epicoma Myrtaceae Paradrallia (2) Fabaceae II Euphorbiaceae Epanaphe (13) Fabaceae Thaumetopoeinae Moraceae (100) Hypsoides (21) Gentianaceae 1 2 3 4 5 6 7 8 Apocynaceae Euphorbiaceae Fabaceae Anaphe (8) Myrtaceae Rubiaceae Sterculiaceae Tiliaceae Notodontidae Gazalina (5) Betulaceae Fagaceae III Anacardiaceae Capparaceae Cistaceae Thaumetopoea (13) Fagaceae Geraniaceae Pinaceae Annu. Rev. Entomol. 2017.62:323-342. Downloaded from www.annualreviews.org Figure 1 Position of the Thaumetopoeinae subfamily within Notodontidae, with the indication of three major clades (roman numerals), the Access provided by Swedish University of Agricultural Sciences on 03/29/17. For personal use only. main genera (n = number of species), main host-plant families, and their geographic distribution. Phylogenetic tree of Notodontidae from Zahiri et al. (150) (1 = Pygaerinae, 2 = Dudusinae, 3 = Phalerinae, 4 = Thaumetopoeinae, 5 = Heterocampinae, 6 = Notodontinae, 7 = Nystaleinae, 8 = Dioptinae). Phylogenetic tree of Thaumetopoeinae from the combined analysis of adult morphology and mitochondrial DNA sequence by Basso (6). The total number of species included in the figure (83) is lower than the expected number (104) because some African and Australian genera were not included. The diverse African and Australian clades are poorly known as far as taxonomy and distribution are concerned (27, 43, 89). The Australian genus Ochrogaster seems to be a complex of species found throughout Australia (27, 39). Almost all of the processionary moth species are associated with trees and shrubs, like most of Notodontidae (84), exploiting a large number of host plants belonging to several families of www.annualreviews.org • Global Change and Processionary Moths 325 EN62CH18-Battisti ARI 22 December 2016 11:31 gymnosperms and angiosperms (7, 28, 105) (Figure 1). The only exception is T. herculeana,which is associated with ground-creeping plants of Cistaceae (Cistus and Helianthemum) and Geraniaceae (Erodium) in dry Mediterranean areas (44, 45). At the species level, processionary moths tend to be polyphagous or oligophagous. The main host plants of species belonging to the Australian clade are many species of Fabaceae (Acacia) and Myrtaceae (Corymbia and Eucalyptus) (39). The host plants of the second clade (Figure 1) are important because they provide food to a number of moth species farmed for silk production in Africa, including Madagascar (28, 80, 81, 97), or the larvae are used as human food (12) and animal feed (55). Species within the third clade (Gazalina spp. and Thaumetopoea spp.) are associated with economically important trees such as Fagaceae (oaks, Quercus), Pinaceae (pines, Pinus), and Anacardiaceae (pistachio, Pistacia) and can occasionally occur at high densities (outbreaks) in the northern part of their range, such as the Mediterranean basin and Europe for Thaumetopoea (7) and the Himalaya foothills for Gazalina (96). A few traits are shared by all species in this