Processionary Moths and Associated Urtication Risk

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 hazards 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 processionary 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.

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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 problems 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 includes 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.

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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

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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 subfamily, most notably the presence of urticating setae on larvae, adults, or both (discussed in detail below). Eggs are laid in clusters, and larvae are gregarious during the entire larval stage. In most species, larvae build silk tents, from which they forage for food in a typical head-to-tail procession. This behavior has been documented for species of each clade, such as T. pityocampa (32, 38), Anaphe spp. (43), and O. lunifer (128).

HEALTH RISKS VARY AMONG TAXA AND THEIR ECOLOGY Urticating setae are found in species from all genera within the subfamily, and thus, these species are potentially harmful to humans and other warm-blooded animals. There are differences among taxa, however, regarding type of setae and their occurrence in different life stages (Figure 2). Setae can occur on larvae, adult females, or both, and setal morphology differs accordingly. Larval setae are short and stiff and occur on each abdominal tergite of mature larvae, reaching a total number of up to 2 million per individual (92). Larval urticating setae can be actively released when the larva is threatened, and this release mechanism probably evolved as a defense against vertebrate natural enemies (8). Adult setae are generally longer and thinner than larval setae and are often bowed (114); they occur on the seventh abdominal tergite and form the so-called anal tuft, which is present in all species of the subfamily (62). They may occur alone (species of clade II) or together with nonurticating, ﬂat, and large scales (species of clades I and III, genus Gazalina), or they can be missing (clade III, genus Thaumetopoea). The adult setae are deposited on the eggs and provide protection of egg masses and possibly of the young larvae that form the colony above the eggs (40, 66). The different setal systems are differentially important with respect to human health effects (Table 1).

Annu. Rev. Entomol. 2017.62:323-342. Downloaded from www.annualreviews.org Species within the Australian clade (Epicoma and Ochrogaster) carry setae as larvae as well as adults. Reactions in humans following direct contact with egg batches covered with setae have been documented for O. lunifer (21, 124, 125) (Table 1), but most attention has been on harmful Access provided by Swedish University of Agricultural Sciences on 03/29/17. For personal use only. effects on domesticated animals. In particular, abortion occurs in mares that accidently ingest larvae that move on the ground (e.g., when changing feeding sites or when dispersing to pupate) (92). This phenomenon has caused considerable economic loss to the horse industry in Australia and has initiated intense research on mechanistic explanations for the abortion (25, 26, 131, 132). The case has some similarity with what has been observed in the United States in relation to larvae of the eastern tent caterpillar, Malacosoma americanum (Lasiocampidae) (146), although the setae carried by this species differ from the urticating ones typical of the processionary moths (37). Species belonging to the African clade (Anaphe, Epanaphe, Hypsoides, Paradrallia) carry setae only as adults. There are no reports on accidental exposure due to adults being attracted to light, even though this seems very likely to happen in situations of high insect density (70). When

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Ochrogaster

Epicoma ?

Paradrallia

II Epanaphe

Hypsoides

Anaphe Annu. Rev. Entomol. 2017.62:323-342. Downloaded from www.annualreviews.org

Gazalina ?

Access provided by Swedish University of Agricultural Sciences on 03/29/17. For personal use only. III

Thaumetopoea

Figure 2 Occurrence and position of urticating setae in larvae and female moths of main genera of Thaumetopoeinae. Red color of ovals and circles indicates the veriﬁed occurrence of urticating setae whereas rose color indicates the likely occurrence. Light gray color of larvae indicates the likely shape and size, as precise descriptions are not available.

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Table 1 Impact on animal and human health of setae from processionary moths (adults and larvae) from different geographic areas

Species Stage Target Impact Reference(s) Australia Epicoma melanosticta NA Humans Dermatitis 59 Epicoma sp. Larva Humans Dermatitis 125 Ochrogaster lunifer Larva Guinea pigs Abortion 73, 121 (lab) Ochrogaster lunifer Larva Horses Mare abortion 23, 25, 26, 131, 132 Ochrogaster lunifer Larva Humans Dermatitis 21, 59, 124, 125 Ochrogaster lunifer Larva Humans Ophthalmia 21, 124, 125 Ochrogaster lunifer Adult Humans Pediatric osteomyelitis 136 Tanystola isabella Adult Humans Dermatitis 114 Trichiocercus sp. Larva Humans Dermatitis 125 Africa and Madagascar Anaphe panda (= infracta) Adult Humans Dermatitis 43, 59, 95 Anaphe reticulata (= ambrizia) Adult Humans Dermatitis 59, 95 Anaphe venata Adult Humans Dermatitis 43, 59, 66, 69, 70, 95, 114 Epanaphe moloneyi Adult Humans Dermatitis 59, 95, 114 Hypsoides semifusca Adult Humans Dermatitis 28 Hypsoides singularis Adult Humans Dermatitis 28 Asia (Himalaya) Gazalina apsara (= venosata) Unknown Humans Dermatitis 59, 114 Gazalina chrysolopha Adult Humans Panuveitis (blindness in 77 children) Gazalina sp. Adult Humans Dermatitis 114 Europe and Mediterranean Thaumetopoea herculeana Larva Humans Dermatitis and allergy 7, 59, 86 Thaumetopoea jordana Larva Humans Dermatitis and allergy 7, 59, 86 Thaumetopoea pinivora Larva Humans Dermatitis and allergy 7, 36, 53, 54, 59, 86 Thaumetopoea pinivora Larva Humans Ophthalmia 126 Thaumetopoea pityocampa/wilkinsoni Larva Cats Pododermatitis 86, 99 Thaumetopoea pityocampa/wilkinsoni Larva Cats Ptyalism, glossitis, and 86, 99 Annu. Rev. Entomol. 2017.62:323-342. Downloaded from www.annualreviews.org tongue necrosis Thaumetopoea pityocampa/wilkinsoni Larva Cats Conjunctivitis 86

Access provided by Swedish University of Agricultural Sciences on 03/29/17. For personal use only. Thaumetopoea pityocampa/wilkinsoni Larva Dogs Conjunctivitis 19, 86, 99 Thaumetopoea pityocampa/wilkinsoni Larva Dogs Ptyalism; glossitis; lips, 14, 19, 86, 90, 91, 99, 149 nose, and tongue necrosis Thaumetopoea pityocampa/wilkinsoni Larva Dogs Dermatitis, angioedema 14, 86, 99 Thaumetopoea pityocampa/wilkinsoni Larva Dogs, cats Respiratory impairment 86, 99 Thaumetopoea pityocampa/wilkinsoni Larva Guinea pigs Dermatitis and ophthalmia 50 (lab) (Continued )

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Table 1 (Continued )

Species Stage Target Impact Reference(s) Thaumetopoea pityocampa/wilkinsoni Larva Horses Dermatitis, tongue necrosis 86 Thaumetopoea pityocampa/wilkinsoni Larva Humans Dermatitis and allergy 7, 35, 50, 59, 67, 86, 106, 107, 138, 140, 142, 148 Thaumetopoea pityocampa/wilkinsoni Larva Humans Ophthalmia 50, 126, 145 Thaumetopoea pityocampa/wilkinsoni Larva Humans Pediatric osteomyelitis 144 Thaumetopoea pityocampa/wilkinsoni Larva Humans Dermatitis in children, 4, 42, 122, 143 systemic Thaumetopoea pityocampa/wilkinsoni Larva Humans Dermatitis in adults 16, 29, 141 Thaumetopoea pityocampa/wilkinsoni Larva Humans Occupational dermatitis 137 Thaumetopoea pityocampa/wilkinsoni Larva Humans Anaphylactic shock 56, 139 Thaumetopoea pityocampa/wilkinsoni Larva Humans Hypertension and 64 abdominal pain Thaumetopoea pityocampa/wilkinsoni Larva Pigs Face edema, rhinitis, 99 tongue necrosis Thaumetopoea pityocampa/wilkinsoni Larva Ruminants Tongue necrosis, edema 86, 99 Thaumetopoea processionea Larva Dogs Ptyalism, glossitis, and 57 tongue necrosis Thaumetopoea processionea Larva Dogs Conjunctivitis 57 Thaumetopoea processionea Larva Dogs Stomatitis 57 Thaumetopoea processionea Larva Dogs Respiratory impairment 57 Thaumetopoea processionea Larva Horses Ptyalism, glossitis, and 57 tongue necrosis Thaumetopoea processionea Larva Horses Conjunctivitis 57 Thaumetopoea processionea Larva Horses Stomatitis 57 Thaumetopoea processionea Larva Horses Respiratory impairment 57 Thaumetopoea processionea Larva Humans Dermatitis and allergy 7, 59, 68, 76, 78, 85, 86, 88, 135 Thaumetopoea processionea Larva Humans Ophthalmia 126 Thaumetopoea processionea Larva Humans Anaphylactic shock 17, 72 Thaumetopoea processionea Larva Humans Dermatitis in children 46, 47, 75 Thaumetopoea processionea Larva Humans Dermatitis in adults 51

Annu. Rev. Entomol. 2017.62:323-342. Downloaded from www.annualreviews.org Thaumetopoea processionea Larva Ruminants Tongue necrosis 18 Thaumetopoea solitaria Larva Humans Dermatitis and allergy 7, 59, 86 Access provided by Swedish University of Agricultural Sciences on 03/29/17. For personal use only. NA indicates that the data are not available.

the moth is farmed for silk in Africa, the silk is extracted from the larval nests under controlled conditions. Cocoon spinning and adult emergence occur within these nests. When female moths emerge, some setae will dislodge, contaminating the silk. In A. panda, the nest is soaked in water for a half hour to remove the urticating setae contained in the silk (119). Workers involved in the extraction process may suffer reactions from these setae (43) (Table 1). The Asian species of Gazalina carry setae in the adult females. These may be released inci- dentally when adults are attracted to lights, generating serious skin reactions and even blindness

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in children who come in contact with them (77) (Table 1). The larvae of this group have not yet been studied, but one could suspect that they carry setae; in G. chrysolopha, dorsal structures similar to those in larvae of Thaumetopoea spp. (so-called mirrors) have been described (15). Insect allergens: molecules, generally Most information on detrimental effects of setae comes from species within Thaumetopoea, proteins, produced by in particular T. pityocampa (86) (Table 1). In Thaumetopoea species, only the larva carries setae. insects and able to Ovipositing females cover egg batches with scales but not setae. People can be exposed to setae activate an immune either through direct contact with larvae or their cast-off exuviae (8) or through contact with setae response in the spread by the wind (68, 75, 76, 93, 141). The setae penetrate the skin into the peripheral blood receiving organism vessels, and attachment is guided by hook-like structures (67). Or the setae can enter the eyes Range expansion: (54, 76, 141) or, less frequently, the respiratory system (122, 138). Reactions in humans can be expansion of the distribution range of a strong and painful (86). Vulnerability varies among individuals (142). Domestic pets (cats, dogs) species associated with and farm animals (cattle, goats, horses, pigs, sheep) can be affected, either through direct contact dispersal, either active with larvae or their tents or by ingesting setae left on pasture during processions (86). Recent or passive, into an research indicates that certain proteins in the setae are insect allergens (13, 106, 107). unoccupied habitat The risk of humans and domesticated animals being affected by setae from processionary moths in natural habitats is directly related to insect population density. For most species, little is known about their population dynamics. High densities (outbreaks) occur, with varying frequency, in T. pityocampa (71), T. processionea (63, 85), and T. pinivora (24). In outbreak situations, a signiﬁcant proportion of the human population shows symptoms (141). O. lunifer can occur at high densities (41), and the problem with mare abortion seems to be related to unusually high larval density (92). G. chrysolopha has been reported to outbreak in evergreen forests in Pakistan and Nepal, and health problems due to high densities of moths attracted to lights most likely refer to outbreak situations (77). An indirect effect of processionary moths was a change in the perception of pine trees in the Balearic Islands after the moth invasion and subsequent high population density. People developed a highly negative opinion of these trees because of the association with the reactions caused by the larvae and often preferred to remove the trees rather than taking the risk of being exposed to the setae (129).

IS THERE A RISK THAT HEALTH PROBLEMS WILL INCREASE WITH CLIMATE CHANGE? Considering the wide distribution of processionary moths and the considerable impacts they may have on plant, human, and domesticated animal health, one could ask the question of whether global change is increasing the risk of exposure. To evaluate species responses to climate change, it is necessary, whenever possible, to separate the effects on range expansion/contraction from those

Annu. Rev. Entomol. 2017.62:323-342. Downloaded from www.annualreviews.org on population dynamics (9). Although historical data on geographical occurrence can be retrieved relatively easily from surveillance programs, in particular for pest species (e.g., Thaumetopoea spp.) (48, 109), the variation in mortality factors determining population dynamics, such as weather, Access provided by Swedish University of Agricultural Sciences on 03/29/17. For personal use only. is much more difficult to obtain (5). Thus, range expansion is rather easy to track, whereas the effects of climate change on population dynamics remain less well studied, and they will continue to be so unless specific research programs are developed. The case of the pine processionary moth in Europe is a prime example of insects responding to climate change. This species was originally restricted to the Mediterranean area. The larvae have the unusual habit of developing through the winter. Feeding takes place whenever suitable weather conditions are met; during the cold winter months, critical conditions include warming tent microclimate as a result of solar radiation to a temperature above 9◦C during the day whereas air temperature during nights needs to be above 0◦C(Figure 3) (11). Despite their supercooling point being −7◦C, larvae can tolerate temperatures as low as −17◦C, as their body fluids can

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Winter larval feeding Summer adult dispersal

T>14˚C

IfT>9˚C and T>0˚C

Elevation/latitude Climate range expansion change Feeding activity Feeding

T ˚C

Figure 3 Interactions between temperature and the life history of the pine processionary moth Thaumetopoea pityocampa. In winter, the larvae beneﬁt from both solar radiation during the day and temperatures above 0◦C during the night, and the combination of both makes them start feeding. In summer, moths beneﬁt from warmer nights by increasing their activity and dispersal. Global warming is facilitating the range expansion of the moth to higher elevations/latitudes. Data from Battisti et al. (10, 11).

freeze and unfreeze (52). The milder the winter, the better the performance and the more likely

Annu. Rev. Entomol. 2017.62:323-342. Downloaded from www.annualreviews.org the establishment of populations beyond the historical range (20), sometimes exploiting host plants previously not used, such as the mountain pine Pinus mugo in the Alps (127). Temperature is an important factor in T. pityocampa for flight initiation. Females have a takeoff threshold at 14◦C, Access provided by Swedish University of Agricultural Sciences on 03/29/17. For personal use only. and warmer summer nights facilitate flight and expansion outside of the previous range (10). Thus, increased larval survival and improved dispersal conditions have resulted in the species expanding its range latitudinally and altitudinally in south Europe during the last decades (11), and the range will likely continue to expand as long as suitable hosts are available (104). Extreme heat events, however, could result in local extinction in newly established colonies as high temperatures inflict mortality in sensitive life stages, as observed in young T. pityocampa larvae in Europe in 2003 (103). Accidental human transportation of the moth beyond the northern edge of the range during the last decades is another route of range expansion (discussed in detail below). Successful establishment, although facilitated by climate change (101), could indicate that there is still room for expansion as long as moth dispersal and larval survival are not limited by low temperature.

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Old records of T. pityocampa in mountainous areas, into which it is currently expanding [cf. the locus typicus in Tyrol (33)], may indicate a distribution that has been waxing and waning over time as an effect of climatic fluctuations. Current climate change could well be considered a forced waxing of the distribution. The effect on the population dynamics, in both core and expansion areas, however, remains to be explored. The few data available do not suggest a clear temperature effect during the last 40 years on the dynamics either in the southern Alps (130) or in France (71). Outbreaks started in the expansion area of both the Paris basin and the southern Italian Alps, exacerbated by the absence of natural enemies (4, 116). Such outbreaks will likely continue as long as weather is favorable, and natural enemies, or human activities, do not reduce density to endemic levels. In situations such as these, climate warming has influenced both expansion and dynamics, the latter due to enemy-free space that will probably last for a limited period only (4). An indication of the flexible phenology of the species is the 1997 finding in coastal Portugal of a population that has shifted to larval development in summer (94). The shift has been associated with an increased larval tolerance to high temperature (118) and represents a case of allochronic speciation (117). It is not clear whether climate change is responsible for the shift, but climate certainly plays a key role in the process (60). With what is known for T. pityocampa, one may suspect that the recent outbreaks of T. pinivora (24) and T. processionea (48) at the northern edge of their ranges in Europe could also be attributed to climate change. One can gather from current knowledge [data on supercooling points in overwintering eggs for T. processionea (82)]thatitis very unlikely that climate change per se has contributed to recent outbreaks. As for the other species of processionary moths, there are no data available to suggest that climate change has contributed to range expansion or changed population dynamics. Consequently, there are no data on climate change–related increases in health risks for species other than T. pityocampa. We recognize, however, that in the last 20 years there has been an increase in the report- ing of setae-related health problems associated with several processionary moth species (Table 1). There is no evidence, however, that other processionary moths should be similarly affected. Possi- bly, G. chrysolopha in Himalaya could respond positively to climate warming because the life history seems similar to that of T. pityocampa; specifically, the larvae feed across the cold season on evergreen species of Quercus and Alnus, resting in silk tents during the day and foraging nocturnally (96).

RISKS ASSOCIATED WITH PLANT TRANSPORTATION INTO NEW HABITATS AND CLIMATE WARMING Studies conducted in the last 20 years have revealed several examples of dispersal of Thaumetopoea species outside their natural range with consequences to local human and domesticated animal

Annu. Rev. Entomol. 2017.62:323-342. Downloaded from www.annualreviews.org populations (3, 99). In T. pityocampa, pioneer colonies found in the early 2000s beyond the front edge of the moth expansion in France were shown to result from human-mediated translocations rather than from natural dispersal of the moth (101). Congruent mitochondrial DNA and mi- Access provided by Swedish University of Agricultural Sciences on 03/29/17. For personal use only. crosatellite analyses assigned most colonies to source populations located at least 260 km away (i.e., in southern France, Spain, or Italy) (60). This finding is clearly inconsistent with the limited flight capabilities of the female moths (7). In addition, the first occurrence of T. pityocampa in Germany, in 2007, probably was the result of an accidental introduction of plant material from a moth population in eastern France approximately 170 km away (49). It is likely that the trade of mature pine trees, transplanted with soil and including pupae, is the pathway for these long- distance jumps (109). The absence of egg parasitoids and the presence of pupal parasitoids in the newly established colonies support this conjecture (101). Moreover, all colonies have been found in human-made habitats within recent plantations of large pine trees (e.g., along highways and urban buildings and in roundabouts and recreation parks) (109, 113, 115). Adult moths attracted

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to light in England in the 1980s probably originated from introductions with plant material, but these insects could not establish at that time (34). Human-mediated introductions have also taken place in Mediterranean islands such as the Balearic Islands and Sardinia; genotyping suggested a Human-mediated likely origin from the nearest mainland (61). In Sardinia, an association with transplant of large dispersal: inadvertent potted trees was evident (74). Similar long-distance jumps have recently been observed in Greece translocation of a (5a) and in southern Russia (121a). species into a novel A simulation of human-mediated translocations in France indicated an increase since 1995 in geographic area the probability of establishment of moth colonies (104). Whereas the harsh winter conditions because of individuals being accidentally would have prevented the establishment of the moth outside its range before the 1990s, winter hidden in commodities warming is making it possible now in large parts of Europe [i.e., where mean minimum temperature from October to March is above 3.3◦C (104)]. Urban areas are even more favorable to the establishment of the moth because the larvae survive significantly better, likely because of the heat island effect (102). Such processes led the moth to colonize highly populated areas, increasing the threat for human health. Thus, human-mediated dispersal leading to the creation of satellite populations will probably accelerate significantly the spread of the pine processionary moth in the future (104), with ornamental trees located outside forests acting as relays for expansion (113). This process may generate new genetic combinations when naturally expanding and introduced populations merge (60). Commercial movements of infested nursery trees have resulted in long-range translocations of the oak processionary moth T. processionea (48, 85) but in this case, in the egg stage. The species, native to continental Europe, has been repeatedly found in the United Kingdom, first in 2006 on a consignment of oak trees (Q. robur) grown in Italy, shipped from the Netherlands in 2004, and planted in London (134). A second record occurred in 2010 involving an imported Q. robur tree; by that year, the infested zone had expanded to reach 120 km2 (133). By contrast, human- mediated dispersal is considered unlikely to explain the scattered distribution of the northern pine processionary moth T. pinivora; a large-scale population genotyping exercise did not indicate that this had happened (24). Human-mediated movements of larvae may happen in some species farmed for silk and food in Africa. H. singularis, H. semifusca,andA. aurea are reared in semiagricultural settings in Mada- gascar (28, 98). Farming using Anaphe and Epanaphe species is also practiced among local communities in Kenya [using A. panda reared on Bridelia micrantha (79, 81, 119)], Nigeria [using A. venata, A. infracta,andE. moloneyi (1)], Uganda [using A. reticulata (58)], Cameroon [using E. carteri and E. vuilleti (22)], and Ethiopia (147). However, no information is available about the possible transportation of these species over long distances. Modeling of the potential for further expansion, or establishment when transported over

Annu. Rev. Entomol. 2017.62:323-342. Downloaded from www.annualreviews.org long distances, with regard to climate change has been attempted for T. pityocampa. Climate matching with the species’ phenology was first used to define such climate models, ranging from simple and descriptive (7) to more sophisticated ones (65). In addition, dispersal models based Access provided by Swedish University of Agricultural Sciences on 03/29/17. For personal use only. on reaction-diffusion equations integrating moth flight capabilities, larval response to changing climate parameters, and density of host trees have been developed (102, 111, 112). In the last 5 years, these models began to include the effects of random human-mediated transportations in the spread scenarios (104). Ultimately, attempts were made to develop online tools to predict the risks for human and domesticated animal health at local scale with regard to climate scenarios (110). Overall, the models indicated that the major part of France has already become favorable to the establishment of T. pityocampa colonies (104), and it was predicted that an increase in temperature of 2–3◦C, on average, would expand this favorable area to cover all of western Europe, including England, and a large part of central Europe (111). Moth natural dispersal is strongly constrained

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by the limited dispersal capabilities of adult females [a few dozen meters up to 10.5 km in ﬂight mills (7)], preventing an immediate follow-up of the expansion of the favorable area. However, the modeling results also suggested that moth dispersal at the front edge of the expansion is not purely diffusive but includes long-distance dispersal events (111). Actually, the combination of human-mediated dispersal and climate change is likely to accelerate the expansion process and allow moth colonies to establish in areas far from the expansion front edge. Under the current scenario of global change, it is likely that impacts of the pine processionary moth on human and domesticated animal health will increase as long as the range expands. It remains to be seen, however, to what extent health effects caused by other species will also become more common due to human-mediated dispersal.

SUMMARY POINTS 1. Empirical evidence strongly supports the notion that survival of the pine processionary moth Thaumetopoea pityocampa is favored by global change (climate warming and increased global trade), and thus, the expansion of negative effects of urticating setae into novel areas is also favored by global change. 2. Other processionary moth species are probably similarly favored by global trade, but such impacts are documented only for Thaumetopoea processionea (accidentally dispersed with plants). 3. This review summarizes, for the first time, the presence of urticating setae on different life stages (larva and female moth) on all known Thaumetopoeinae species and the variation in setae location among taxa within the subfamily. 4. The risk for setae causing reactions in humans and domesticated animals is strongly related to density of the life stage (larva or adult) that carries the setae. 5. Modeling data indicate that the global change–driven expansion, and thus further spread of health hazards, in T. pityocampa will most likely continue in the future as long as temperature and human trade increase. 6. There are an increasing number of reports on health hazards from other processionary moth species, particularly a well-studied species, Ochrogaster lunifer, that inflicts mare abortion in horses that accidentally ingest setae-carrying larvae. However, the reviewed literature does not allow any firm conclusions about causal relationships with global change in Thaumetopoeinae species other than T. pityocampa. Annu. Rev. Entomol. 2017.62:323-342. Downloaded from www.annualreviews.org Access provided by Swedish University of Agricultural Sciences on 03/29/17. For personal use only. FUTURE ISSUES 1. The ongoing expansion of Thaumetopoea pityocampa in France into areas with fragmented occurrences of the host tree has raised the question of selection in density or quality of setae. The hypothesis is that there should be selection for lower density, or quality, of setae in areas where host trees are far apart. The reason is that larvae with lower density or quality of setae would invest proportionally more into resources important for the flight capacity of the emerging female (moths disperse directly without feeding). Thus, the prediction to be tested is that the larvae in the expansion area carry fewer and less harmful setae than the larvae in the core area carry.

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2. An increasing amount of literature shows larvae of Ochrogaster lunifer inﬂict serious disease in horses in Australia; mares that accidentally ingest larvae abort their foals, which causes the horse owners considerable economic cost. Thus, much knowledge has been accumulated about the mechanisms behind the abortion in horses. It is reasonable to assume that other warm-blooded animals also can accidentally ingest larvae with their setae in situations when moth density is high. However, very little, if anything, is known about such possible health problems. 3. There is very strong support for the expansion of T. pityocampa being causally linked to climate change. Among other processionary moths, Gazalina chrysolopha, a pest of broadleaved trees in Himalaya, develops through the winter like T. pityocampa. It would be productive to understand whether health hazards recently reported to be caused by G. chrysolopha in Nepal can be linked to pest resurgence associated with climate change.

DISCLOSURE STATEMENT The authors are not aware of any afﬁliations, memberships, funding, or ﬁnancial holdings that might be perceived as affecting the objectivity of this review.

ACKNOWLEDGMENTS We would like to acknowledge Myron P. Zalucki for valuable comments on earlier drafts of the manuscript and two anonymous reviewers for useful comments. Thanks also to Paolo Paolucci for drawing the ﬁgures. The work was partly supported by the University of Padova, the URTICLIM project from ANR France, the Swedish research program Future Forests, and the PCLIM network (international research network about the adaptive response of processionary moths and their associated organisms to global change) that was funded by the ACCAF program of INRA, France.

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Annu. Rev. Entomol. 2017.62:323-342. Downloaded from www.annualreviews.org 93. Petrucco-Toffolo E, Zovi D, Perin C, Paolucci P, Roques A, et al. 2014. Size and dispersion of urticating setae in three species of processionary moths. Integr. Zool. 9:320–27 94. Pimentel C, Calvao˜ T, Santos M, Ferreira C, Neves M, Nilsson JA. 2006. Establishment and expansion Access provided by Swedish University of Agricultural Sciences on 03/29/17. For personal use only. of a Thaumetopoea pityocampa (Den. & Schiff.) (Lep. Notodontidae) population with a shifted life cycle in a production pine forest, Central-Coastal Portugal. For. Ecol. Manag. 233:108–15 95. Pomeroy AWJ. 1921. The irritating hairs of the wild silk moths of Nigeria. Bull. Imp. Inst. 19:311–18 96. Rahman W-U, Chaudhry MI. 1992. Observations on outbreak and biology of oak defoliator, Gazalina chrysolopha Koll. Pak. J. For. 42:134–37 97. Raina SK, Kioko E, Zethner O, Wren S. 2013. Forest habitat conservation in Africa using commercially important insects. Annu. Rev. Entomol. 56:465–85 98. Razaﬁmanantosoa T, Ravoahangimalala OR, Craig CL. 2006. Indigenous silk moth farming as a means to support Ranomafana National Park. Madagascar Conserv. Develop. 1:34–39 99. Riviere` J. 2011. Les chenilles processionnaires du pin: evaluation des enjeux de sant´e animale. PhD Thesis, National Veterinary School of Maisons-Alfort, France

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100. Robinet C, Baier P, Pennerstorfer J, Schopf A, Roques A. 2007. Modelling the effects of climate change on the potential feeding activity of Thaumetopoea pityocampa (Den. & Schiff.) (Lep., Notodontidae) in France. Glob. Ecol. Biogeog. 16:460–71 101. Robinet C, Imbert CE, Rousselet J, Sauvard D, Garcia J, et al. 2012. Warming up combined with the trade of large trees allowed long-distance jumps of pine processionary moth in Europe. Biol. Invas. 14:1557–69 102. Robinet C, Roques A. 2010. Direct impacts of recent climate warming on insect populations. Integr. Zool. 5:132–42 103. Robinet C, Rousselet J, Pineau P, Miard F, Roques A. 2013. Are heat waves susceptible to mitigate the expansion of a species progressing with global warming? Ecol. Evol. 3:2947–57 104. Predictive model 104. Robinet C, Rousselet J, Roques A. 2014. Potential spread of the pine processionary moth on the range expansion in France: preliminary results from a simulation model and future challenges. Ann. For. Sci. of the pine 71:149–60 processionary moth 105. Robinson GS, Ackery PR, Kitching IJ, Beccaloni GW, Hernandez´ LM. 2010. HOSTS. A Database based on climate and of the World’s Lepidopteran Hostplants: Natural History Museum, London, retrieved March 2016. human-mediated http://www.nhm.ac.uk/hosts dispersal. 106. Rodrıguez-Mahillo´ AI, Carballeda-Sangiao N, Vega JM, Garcıa-Ortiz JC, Roques A, et al. 2015. Diagnostic use of recombinant Tha p 2 in the allergy to Thaumetopoea pityocampa. Allergy 70:1332–35 107. Rodriguez-Mahillo AI, Gonzalez-Munoz˜ M, Vega JM, Lopez´ JA, Yart A, et al. 2012. Setae from 106, 107. Identiﬁcation the pine processionary moth (Thaumetopoea pityocampa) contain several relevant allergens. of allergenic proteins Contact Dermat. 67:367–74 from the setae of the pine processionary 108. Roques A, ed. 2015. Processionary Moths and Climate Change: An Update. Dordrecht, Neth.: moth and development Springer of diagnostics. 109. Roques A, Rousselet J, Avci M, Avtzis D N, Basso A, et al. 2015. Climate warming and past and present distribution of the processionary moths (Thaumetopoea spp.) in Europe, Asia Minor and North Africa. In Processionary Moths and Climate Change: An Update, ed. A Roques, pp. 81–162. Dordrecht, Neth.: Springer 108. The ﬁrst published 110. Roques L. 2015. URTIRISK, a software for assessing the allergy risk. In Processionary Moths and Climate synthesis on biology, Change: An Update, ed. A Roques, pp. 402–5. Dordrecht, Neth.: Springer ecology, genetics, 111. Roques L, Rossi J-P, Rousselet J, Berestycki H, Garnier J, et al. 2015. Modeling the spatio-temporal distribution, impact, dynamics of the pine processionary moth. In Processionary Moths and Climate Change: An Update,ed.A and management of the Roques, pp. 227–63. Dordrecht, Neth.: Springer Thaumetopoea 112. Roques L, Soubeyrand S, Rousselet J. 2011. A statistical-reaction-diffusion approach for analyzing processionary moth expansion processes. J. Theor. Biol. 274:43–51 species. 113. Rossi J-P, Garcia J, Roques A, Rousselet J. 2016. Trees outside forests in agricultural landscapes: spatial distribution and impact on habitat connectivity for forest organisms. Landsc. Ecol. 31:243 114. Rothschild M, Reichstein T, Lane NJ, Parsons J, Prince W, Swales SW. 1970. Toxic Lepidoptera.

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Annual Review of Entomology Volume 62, 2017 Contents

Following the Yellow Brick Road Charles H. Calisher pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp1 Behavioral Sabotage of Plant Defenses by Insect Folivores David E. Dussourd ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp15 Neuropeptides as Regulators of Behavior in Insects Liliane Schoofs, Arnold De Loof, and Matthias Boris Van Hiel pppppppppppppppppppppppppppp35 Learning in Insect Pollinators and Herbivores Patricia L. Jones and Anurag A. Agrawal ppppppppppppppppppppppppppppppppppppppppppppppppppp53 Insect Pathogenic Fungi: Genomics, Molecular Interactions, and Genetic Improvements Chengshu Wang and Sibao Wang ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp73 Habitat Management to Suppress Pest Populations: Progress and Prospects Geoff M. Gurr, Steve D. Wratten, Douglas A. Landis, and Minsheng You pppppppppppppp91 MicroRNAs and the Evolution of Insect Metamorphosis Xavier Belles ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp111 The Impact of Trap Type and Design Features on Survey and Detection of Bark and Woodboring Beetles and Their Associates: A Review and Meta-Analysis Jeremy D. Allison and Richard A. Redak pppppppppppppppppppppppppppppppppppppppppppppppppp127

Annu. Rev. Entomol. 2017.62:323-342. Downloaded from www.annualreviews.org Tephritid Integrative Taxonomy: Where We Are Now, with a Focus on the Resolution of Three Tropical Fruit Fly Species Complexes

Access provided by Swedish University of Agricultural Sciences on 03/29/17. For personal use only. Mark K. Schutze, Massimiliano Virgilio, Allen Norrbom, and Anthony R. Clarke ppppp147 Emerging Themes in Our Understanding of Species Displacements Yulin Gao and Stuart R. Reitz ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp165 Diversity of Cuticular Micro- and Nanostructures on Insects: Properties, Functions, and Potential Applications Gregory S. Watson, Jolanta A. Watson, and Bronwen W. Cribb pppppppppppppppppppppppp185 Impacts of Insect Herbivores on Plant Populations Judith H. Myers and Rana M. Sarfraz pppppppppppppppppppppppppppppppppppppppppppppppppppp207

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Past, Present, and Future of Integrated Control of Apple Pests: The New Zealand Experience James T.S. Walker, David Maxwell Suckling, and C. Howard Wearing ppppppppppppppp231 Beekeeping from Antiquity Through the Middle Ages Gene Kritsky pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp249 Phylogeny and Evolution of Lepidoptera Charles Mitter, Donald R. Davis, and Michael P. Cummings pppppppppppppppppppppppppp265 The Ambrosia Symbiosis: From Evolutionary Ecology to Practical Management Jiri Hulcr and Lukasz L. Stelinski pppppppppppppppppppppppppppppppppppppppppppppppppppppppp285 Social Life in Arid Environments: The Case Study of Cataglyphis Ants Rapha¨el Boulay, Serge Aron, Xim Cerd´a, Claudie Doums, Paul Graham, Abraham Hefetz, and Thibaud Monnin ppppppppppppppppppppppppppppppppppppppppppppppp305 Processionary Moths and Associated Urtication Risk: Global Change–Driven Effects Andrea Battisti, Stig Larsson, and Alain Roques pppppppppppppppppppppppppppppppppppppppppp323 African Horse Sickness Virus: History, Transmission, and Current Status Simon Carpenter, Philip S. Mellor, Assane G. Fall, Claire Garros, and Gert J. Venter pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp343 Spatial Self-Organization of Ecosystems: Integrating Multiple Mechanisms of Regular-Pattern Formation Robert M. Pringle and Corina E. Tarnita pppppppppppppppppppppppppppppppppppppppppppppppp359 Evolution of Stored-Product Entomology: Protecting the World Food Supply David W. Hagstrum and Thomas W. Phillips pppppppppppppppppppppppppppppppppppppppppppp379 Ecoinformatics (Big Data) for Agricultural Entomology: Pitfalls, Progress, and Promise Jay A. Rosenheim and Claudio Gratton pppppppppppppppppppppppppppppppppppppppppppppppppppp399 Annu. Rev. Entomol. 2017.62:323-342. Downloaded from www.annualreviews.org Molecular Evolution of Insect Sociality: An Eco-Evo-Devo Synthesis Amy L. Toth and Sandra M. Rehan ppppppppppppppppppppppppppppppppppppppppppppppppppppppp419 Access provided by Swedish University of Agricultural Sciences on 03/29/17. For personal use only. Physicochemical Property Variation in Spider Silk: Ecology, Evolution, and Synthetic Production Sean J. Blamires, Todd A. Blackledge, and I-Min Tso ppppppppppppppppppppppppppppppppppp443

Indexes

Cumulative Index of Contributing Authors, Volumes 53–62 ppppppppppppppppppppppppppp461 Cumulative Index of Article Titles, Volumes 53–62 ppppppppppppppppppppppppppppppppppppp467

Contents ix