Annales de la Société Entomologique de France

This is an Accepted Manuscript of an article published by Taylor & Francis in Annales de la Société Entomologique de France (N.S.) on 03/Jun/2019 (on line), available on line: http:www.tandfonline.com/10.1080/00379271.2019.1615386

A remarkableFor Peer life strategy Review in the iberian Only endemic Acinipe segurensis (Bolívar, 1908) (, )

Journal: Annales de la Société Entomologique de France

Manuscript ID TASE-2019-0012.R2

Manuscript Type: Original Article

Date Submitted by the 30-Apr-2019 Author:

Complete List of Authors: García, Maria Dolores; Universidad de Murcia Facultad de Biologia, Zoology and Physical Antropology Clemente, Eulalia; Universidad de Murcia Facultad de Biologia, Zoology and Physical Anthropology Gómez, Ricardo; Universidad de Castilla-La Mancha - Campus de Albacete Presa, Juan; Universidad de Murcia, Facultad de Biología, Zoology and Physical Anthropology

Keywords / Mots-clés: life cycle, nymphal morphology, Pamphagini, nymphal development

The first data on the developmental life cycle of Acinipe segurensis (Bolívar, 1908) are provided as well as a morphological description of the nymphal stages. Data provided refer to the number of nymphal stages in the two sexes and their duration. The species hibernate in the egg stage. Males undergo four nymphal stages before reaching the adult stage while females undergo five, the extra stage being the third one. Morphological Abstract: features studied concerning the number of antennal segments, the morphology of the wing rudiments on lateral lobes of the meso- and metanotum and the morphology of the external genitalia both in male and female, allowed to briefly describe and illustrate the different nymphal stages. The life cycle is different from other Pamphagini species as concerns the hibernation period and the rate of nymphal growth. A discussion on the possible causes of such divergences is given.

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1 2 3 A remarkable life strategy in the Iberian endemic Acinipe segurensis (Bolívar, 4 5 1908) (Orthoptera: Pamphagidae) 6 7 8 Maria Dolores García1*, Eulalia Clemente1, Ricardo Gómez2 & Juan J. Presa1 9 1 Area of Zoology. Department of Zoology and Physical Anthropology. Faculty of Biology. University of Murcia. 10 11 30100 Murcia. Spain 12 2 Department of Agroforestry and Genetics Technology. Agronomists Higher School. University of Castilla-La 13 Mancha. Albacete University Campus. 02071 Albacete. Spain 14 * Corresponding author : [email protected] 15 16 17 Abstract. The first data on the developmental life cycle of Acinipe segurensis (Bolívar, 1908) are provided as well as 18 For Peer Review Only a morphological description of the nymphal stages. Data provided refer to the number of nymphal stages in the two 19 20 sexes and their duration. The species hibernate in the egg stage. Males undergo four nymphal stages before reaching 21 the adult stage while females undergo five, the extra stage being the third one. Morphological features studied 22 concerning the number of antennal segments, the morphology of the wing rudiments on lateral lobes of the meso- and 23 24 metanotum and the morphology of the external genitalia both in male and female, allowed to briefly describe and 25 illustrate the different nymphal stages. The life cycle is different from other Pamphagini species as concerns the 26 hibernation period and the rate of nymphal growth. A discussion on the possible causes of such divergences is given. 27 28 29 Résumé. Une stratégie de vie remarquable chez Acinipe segurensis (Bolívar, 1908), endémique ibérique 30 (Orthoptera : Pamphagidae). Les premières données sur le cycle biologique de Acinipe segurensis (Bolívar, 1908) 31 sont fournies, ainsi qu'une description morphologique des stades nymphaux. Les données fournies font référence au 32 33 nombre de stades nymphaux chez les deux sexes et à leur durée. Cette espèce hiberne au stade œuf. Les mâles passent 34 par quatre stades nymphaux avant d'atteindre le stade adulte, tandis que les femelles passent par cinq stades, le stade 35 supplémentaire étant le troisième. Les caractéristiques morphologiques étudiées concernant le nombre de segments 36 37 antennaires, la morphologie des ébauches alaires sur les lobes latéraux du méso- et métanotum et la morphologie des 38 organes génitaux externes chez le mâle et la femelle permettent de décrire et illustrer les différentes phases nymphales 39 chez les deux sexes. Le cycle de vie observé est différent du reste des espèces de Pamphagini en ce qui concerne la 40 période d'hibernation et le taux de développement des nymphes. Une discussion sur les causes possibles de telles 41 42 divergences est présentée. 43 44 Keywords: life cycle, nymphal morphology, nymphal development, Pamphagini. 45 46 47 Acinipe segurensis (Bolívar, 1908) is a Pamphagidae species endemic to the Iberian Peninsula and restricted 48 49 to its Southern Mediterranean area (Llorente & Presa 1997). It is typical in places abounding with rosemary, 50 where it lives feeding almost exclusively on the leaves of Rosmarinus officinalis L. 51 As usual, the studies on the biology and development of Pamphagidae are very scarce, particularly in 52 53 comparison with those devoted to orthopteran species of economic interest. Nevertheless, the biology and 54 development features of certain species, such as elephas (Linnaeus, 1758), 55 56 rhodanica Uvarov, 1923, Euryparyphes sitifensis Brisout, 1854, Acinipe hesperica Rambur, 1838, 57 Acrostira euphorbiae García & Oromí, 1992 and Pamphagus marmoratus Burmeister, 1838 and 58 59 Pamphagus sardeus (Herrich-Schäffer, 1840) are known (Aiouaz & Boufersaqui 1973; Foucart & Lecocq 60 1996; Korsakoff 1941; Llorente 1990; López et al. 2007; Massa & Cusimano 1979 respectively).

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1 2 3 Concerning the biology and behaviour of A. segurensis, a recent work due to Gómez Ladrón de Guevara et 4 al. (2009) described population abnormal outbreaks that can produce significant vegetation damages, an 5 6 unusual phenomenon among Pamphagidae (Mendizábal 1948; Massa & LoVerde 1990; Foucart & Lecoq 7 1996; Llorente & Presa 1997; Bounechada & Doumandji 2003; Massa et al. 2012). 8 9 Gómez et al. (2010) studied the species in nature for two consecutive years and pointed that the eggs hatch 10 during the following spring after oviposition; so the life cycle seems to suffer diapause during the egg stage 11 12 instead of entering diapause in larval stage, a characteristic feature of Pamphagini (Korsakoff 1941; Aiouaz 13 & Boufersaqui 1973; Massa & Cusimano 1979; Llorente 1990; Foucart & Lecocq 1996; López et al. 2007). 14 15 With reference to behavioral aspects, García et al. (2014) described its sound producing mechanism, which 16 shows certain differences from those known up to now in other brachypterous species of Pamphagidae, as 17 well as the physical song features of song produced by females. 18 For Peer Review Only 19 Taking into account the peculiarities that the life cycle of A. segurensis seems to present besides the 20 devastating effects that its populations sometimes have, a study in captivity was carried out to know the 21 22 life cycle features of this species. The data here provided may be of great interest for a possible population 23 control as well as for trying to explain the causes of divergences observed respect to other species of the 24 25 same genus and the tribe Pamphagini. 26 27 Materials and methods 28 29 A total of 36 females and 44 males, in nymphal stage, were collected in Monte del Portillo (38°20' 25"N 2°19'20"W), 30 Yeste's municipal area (Albacete), located 800 metres a.s.l. The vegetation is composed of pine forest of Aleppo (Pinus 31 halepensis Mill.) with undergrowth of abundant rosemary (Rosmarinus officinalis) and thyme (Thymus vulgaris L.) 32 33 belonging to the Sector Manchego-Murciano (Gómez et al. 2010). Captures were made by hand on the plants or with 34 an entomological net in April-May of 2012 and 2013. As the first moult coincides with hatching and were 35 collected in the field after hatching, developmental stages were recorded starting with the first mobile nymph (Foucart 36 & Lecoq 1996; Schultner et al. 2012: Elamin et al. 2014). 37 38 After collection, each individual was placed in a small glass jars, identified with a number, with the top perforated. 39 Individuals were fed with lettuce (Lactuca sativa L.) and rosemary (R. officinalis). Water was added by spraying food 40 “ad libitum”. Heat was provided with 40 w light bulbs lit for 16 hours a day for all the period. Every jar was reviewed 41 42 every two days; food was changed and water added at that moment. 43 The number of instars and instars duration were measured separately for each individual by recording the number of 44 developmental stages and the days elapsed between successive moults. Data were analyzed with IBM® SPSS® 45 46 Statistics 20 software. 47 Exuviae were kept independently by identifying the number of the specimen and the date of the moult. Faeces were 48 collected after each moult and stored identifying the number of the specimen and the corresponding moult. In addition 49 the feeding behaviour of individuals was studied by direct observation. 50 51 During the development period the temperature remained between 20°C and 32,2° C and the relative humidity between 52 31,2% and 60%. 53 According to Llorente (1990), three growth features were registered per individual and instar to describe it: 1) the 54 55 number of antennal segments, 2) the morphology of the wing rudiments on lateral lobes of the meso- and metanotum 56 (tegmina and wings of the adult) and 3) the morphology of the external genitalia both in male and female. 57 58 59 Results 60

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1 2 3 Of the 80 nymphs collected (44 males, 36 females), only 18 males and 17 females reached the adult stage. 4 The remaining nymphs died at different stages. 5 6 Males and females of A. segurensis pass through different number of nymphal stages before reaching the 7 adult stage. Males pass through four stages and females through five, the extra stage of females being the 8 9 third one. As usual among Pamphagidae, the reversal of the wingrudiments occurs in the antepenultimate 10 stage, that is, the third (moult II-III) in males and the fourth (moult III-IV) in females. 11 12 On average, females developed from egg to adult in 44.3 days and males in 34.6 days (Table 1). 13 As can be seen, the length of each intermoult period was very variable. Results of U-Mann-Whitney tests 14 15 applied did not show significant differences between the length of each stage in both sexes except when 16 comparing the stage IV of males and females, which offers a significant difference (Mann-Whitney U test, 17 U=66.50, p=0.003). Nevertheless, when comparing data from the two consecutive years, the two first stages 18 For Peer Review Only 19 (I and II) showed differences concerning its duration, both in males (Mann-Whitney U test, U=17.50, 20 p=0.043; U=18.00, p=0.055, respectively) and in females (Mann–Whitney U test, U = 16.0, p=0.059; 21 22 U=2.50, p<0.001, respectively), although such differences are only marginally significant for stage II of 23 males and for stage I of females. 24 25 From a morphological point of view, the different nymphal stages are easily recognizable in both 26 sexes by the studied features. 27 28 29 Nymph I 30 Male. Ensiform and flattened antennae composed of seven flagellomeres (Figure 1A). Sometimes, the third 31 32 flagellomere may show a transversal groove in the middle. Wing buds barely sketched, with rounded lower 33 edge (Figure 1B). Subgenital plate narrowed to apex, which is V-notched, with short lobes (Figure 1C). 34 35 Female. Antennae as in the male, ensiform and flattened, composed of seven or eight flagellomeres 36 depending on whether the third is divided (Figure 2A) or only presents a groove. Wing buds as in the male 37 38 (Figure 2B). Upper ovipositor valves short and obtuse, separated by a nick at angle. Lower ovipositor valves 39 widely triangular, occupying a third of the sternite (Figure 2C). 40 41 42 Nymph II 43 Male. Ensiform antennae composed of seven / eigth flagellomeres in which grooves already appear marking 44 45 future divisions, especially in the segments 3, 6 and 7 (Figure 1D). Wing rudiments clearly differentiated, 46 the mesothoracic one rounded directed backwards, the metathoracic one more clearly distinguishable than 47 48 in the previous stage. Both wing buds and lateral lobes show longitudinal ridges that will later be the veins 49 (Figure 1E). Subgenital plate, in ventral view, even more narrowed to apex, the notch smaller and more 50 closed, slightly curve (Figure 1F). 51 52 Female. Antennae strongly ensiform, similar to those of stage I, although some grooves appear in 53 flagellomeres 3, 6 and 7 (Figure 2D). Wing buds very weak. Mesothoracic lobe slightly directed obliquely 54 55 downwards. Metathoracic lobe almost identical to that of previous stage (Figure 2E). Upper ovipositor 56 valves more acute and long, their inner edges are parallels. The inner valves, small but distinguishable, are 57 58 between them. Lower ovipositor valves reaching the middle of the sternite (Figure 2F). 59 60

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1 2 3 Nymph III 4 Male. Antennae less ensiform than at nymph II, at least at the apical zone, composed of eleven 5 6 flagellomeres with grooves, especially in the most basal segments (Figure 1G). In this stage, the reversal 7 of the wing rudiments has already happened. Tegmen rudiment reversed upward, reaching beyond the 8 9 mesothorax hind edge; wing located behind tegmen, well differentiable, occupying the lower part of 10 metathorax, its upper edge curved (Figure 1H). Apex of subgenital plate parabolic, reaching beyond the 11 12 middle of paraprocts (Figure 1I). 13 Female. Antennae less ensiform than at nymph II, composed of nine flagellomeres, some of them showing 14 15 transversal grooves (Figure 2G). Mesothoracic wing rudiment better definite and well lobate, directed 16 obliquely downwards, not reaching the middle of metathorax; metathoracic wing rudiments well 17 differentiated, directed downwards. In both wing rudiments, outlines of future venation is distinguished 18 For Peer Review Only 19 (Figure 2H). Upper ovipositor valves longer and more slender, addressing with their inner edges parallels 20 at the base. Between them the apex of inner valves can be observed. Lower valves more developed, reaching 21 22 the base of the upper ones (Figure 2I). 23 24 25 Nymph IV 26 Male. Antennae less ensiform than at nymph III, at least at the apical zone, composed of fourteen 27 flagellomeres, the basal ones featuring grooves (Figure 1J). Tegmen rudiment reversed upward, reaching 28 29 beyond the middle of metathorax and reaching the wing tip, showing marks of future veins. Hindwings 30 smaller than the tegmina, with weaker venation, their upper edge curved and thick (Figure 1K). Subgenital 31 32 plate longer than at nymph III, clearly reaching beyond cerci. Paraprocts and epiproct not visible ventrally 33 (Figure 1L). 34 35 Female. Antennae more elongated and less ensiform than at nymph III, composed of thirteen flagellomeres, 36 the basal ones with some grooves (Figure 2J). Reversal of the wing rudiments has already happened. 37 38 Tegmen rudiment directed upwards, reaching beyond the hind mesothoracic edge. Wing rudiment well 39 differentiated, its upper edge curved; it is located behind the tegmen rudiment, occupying the metathorax 40 lower part (Figure 2K). Upper ovipositor valves reaching the middle of the paraprocts. Lower valves 41 42 reaching beyond the middle of the upper ones, not reaching the base of cerci. Inner valves no longer visible 43 (Figure 2L). 44 45 46 Nymph V 47 48 Female. Antennae longer than at nymph IV, still slightly ensiform, at least at base, composed of fifteen 49 flagellomeres, the basal ones with some grooves (Figure 2M). Reversed tegmina rudiment reaching beyond 50 the middle of metathorax and reaching or exceeding the wing rudiment end. Wing rudiments smaller, the 51 52 upper edge curve and thick; their venation weaker (Figure 2N). Upper ovipositor valves reaching beyond 53 the cerci apex. Apex of lower valves reaching the base of cerci, clearly showing a transversal keel. 54 55 Subgenital plate with hind edge similar to that of the adult. (Figure 2O). 56 57 58 Both in male and female nymphs, sometimes appear individuals in which two-stage characteristics are 59 combined, especially in relation to the antennae. 60

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1 2 3 4 Discussion 5 6 Life cycle features 7 The Orthopteran Mediterranean species have a life cycle with hibernation in egg stage and a rapid larval 8 9 development. These features are considered typical of although it is due without a doubt to the 10 fact that most of the species studied live in temperate areas with cold winters (Uvarov 1977). Nevertheless, 11 12 there is a group of species belonging to the Pamphagini tribe which have a cycle absolutely different. They 13 suffer hibernation as nymph, both in nature and in captivity (Uvarov 1967; Massa & Cusimano 1979; 14 15 Llorente 1990; Massa 1990; Massa & Lo Verde 1990; Llorente et al. 1995; Bounechada et al. 2006, among 16 others). 17 Observations both in field (Gómez et al. 2010) and in laboratory (results here presented), have stated that 18 For Peer Review Only 19 A. segurensis has a life cycle with hibernation in egg stage and a rapid larval development. These features 20 in principle separate it from the rest of Pamphagini species, which are characterized by a long egg 21 22 incubation period and a low rate of larval growth (Uvarov 1967), their larval development ranging between 23 4 and 12.5 months (Llorente & Presa 1997). 24 25 Nevertheless, in some Pamphagini species it has been described or suggested that, under certain 26 circumstances or in some areas, they can vary their life cycle in a way that would resemble that here 27 described for A. segurensis. For example, some species of the genus Ocneridia Bolívar, 1912 inhabiting 28 29 Italy hibernate at nymphal stage (Massa et al. 2012) while, in Algeria, they hibernate at egg stage 30 (Boudegzdame 1980; Bounechada et al. 2006). But in different areas of Algeria, depending on the weather 31 32 conditions throughout the year, it has been noted that such species may present one type of hibernation or 33 another (Bounechada et al. 2006). 34 35 In other species, such as the Canary endemic Acrostira euphorbiae, a life cycle is presented with adults and 36 nymphs interspersed throughout the year depending of the phenology of their nourishing plant (López et 37 38 al. 2007). However, the life cycle is not related to the nourishment for other species of the same genus, 39 Acrostira bellamyi (Uvarov, 1922), which presents the same type of life cycle, that is with interspersed 40 adults and nymphs all-year round (Hernández-Teixidor et al. 2014). 41 42 The available data suggest that all the species belonging to the genus Acinipe Rambur, 1838 have a life 43 cycle with nymphal diapause (Descamps & Mounassif 1972; Llorente 1990; Llorente & Presa 1997; Massa 44 45 et al. 2012), but Bounechada et al. (2006) indicate that Acinipe tibialis (Fieber, 1853) falls among the 46 species that may show egg diapause in an Algerian area, although they do not provide any further 47 48 information. 49 The reasons for variations of the life cycle of the different species are diverse. In some cases, as commented 50 above, they are related to the continuous food availability (López et al. 2007), in other cases they are related 51 52 to the macroclimatic conditions, such as the case of the Ocneridia species inhabiting Italy (Massa et al. 53 2012) and Northern Africa (Bounechada et al. 2006), the annual climate fluctuations, especially humidity 54 55 (Bounechada et al. 2006; Guendouz-Benrima et al. 2011), the local adaptations (Guendouz-Benrima et al. 56 2011) and, even, some peculiarities of the embryonic development, such as the presence of embryos with 57 58 “late diapause” and embryos with “premature diapause” [diapause tardive and diapause précoce sensu 59 60

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1 2 3 Boudegzdame (1980)]. Since in no case the authors find a clear determinant factor for these variations, 4 Guendouz-Benrima et al. (2011) consider the possible interaction of some of them. 5 6 7 Number and duration of nymphal stages 8 9 Among the , the number of nymphal stages varies between 4 and 9 due to different causes (Uvarov 10 1977). Available data on Pamphagini are also diverse (Table 2). In some cases, females have an additional 11 12 stage or a longer duration of the last nymphal stage, probably related to their larger size (Uvarov 1977) 13 (Table 2). 14 15 There are few data on the nymphal development duration as well as that of intermoult periods, and the 16 available ones were all obtained in captivity. Taking into account that the environmental conditions have 17 a strong influence in such duration, mainly humidity and temperature (Schädler & Witsack 1999; 18 For Peer Review Only 19 Guendouz-Benrima et al. 2011; Petit 2014), the results are difficult to compare (Table 2). For A. segurensis 20 the intermoult periods and the duration of the whole larval development are much shorter (Table 1), more 21 22 similar to that of some Pamphagidae of tribe Trinchini, as Prionotropis rhodanica Uvarov, 1923 (Foucart 23 & Lecoq 1996) and that of Caelifera with embryonic diapause (Schädler & Witsack 1999). 24 25 The significant differences found regarding the duration of stage IV in males and females seem to be clearly 26 related to that in males it is the preadult stage and in females there is still another nymphal stage. Concerning 27 the significant differences found in the duration of stages I and II between the two years of the study, they 28 29 can be due to the different experimental environmental conditions in both years; in 2012 the mean 30 temperature was 6ºC higher and the mean RH was 20% lower than in 2013. So, these parameters could 31 32 have affected the duration of the stages (Uvarov 1966, 1977; Joern & Gaines 1990; Schultner et al. 2012) 33 34 35 Causes of the life cycle features 36 The differential features of the life cycle of A. segurensis (absence of nymphal diapause) that, in principle, 37 38 separate this species from the rest of Pamphagini, may be due to all or just some of the causes cited above 39 affecting the different species. Nevertheless, when examining in detail such causes it can be seen that some 40 of them do not seem to affect especially this species. 41 42 Variations in life cycle due to changes in climate in the different geographical locations of the species or to 43 interannual climate variation (Bounechada et al. 2006; Guendouz-Benrima et al. 2011; Massa et al. 2012) 44 45 do not seem to be the cause for A. segurensis. Their populations have been followed in Hellín (Albacete) 46 (unpublished data) for ten years and no changes in the cycle have been observed. Its phenology has been 47 48 studied in three different locations, Sierra del Taibilla (Albacete) (Gómez Ladrón de Guevara et al. 1992), 49 Sierra Espuña (Murcia) (García & Presa 1985) and Font Roja (Alicante) (Hernández et al. 1998); in all 50 them the life cycle is the same. It is also interesting to point out that there is no reference to the capture of 51 52 nymphs before April. 53 Telfer & Hassal (1999) propose the possibility of ecotypes with different life cycle depending on the 54 55 different climates in the distribution area. However, many Mediterranean Pamphagidae species have 56 developed physiological adaptations in nymphs and adults in harsh climates but have not changed their 57 58 biological cycle. This indicates that such feature is firmly rooted in their genetic constitution (Uvarov 1967, 59 1977). Furthermore, other species of Pamphagini from the Iberian Peninsula, sympatric with A. segurensis, 60

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1 2 3 such as Ocnerodes brunneri (Bolívar, 1876) (Hernández et al. 1998), Kurtharzia sulcata (Bolívar, 1912) 4 (Gómez Ladrón de Guevara et al. 1992) or monticola (Rambur, 1838) (García & Presa 1985), 5 6 present nymphal diapause in their life cycle; thus, it is possible to consider these populations of A. 7 segurensis with embryonic diapauses as an ecotype. 8 9 It has been mentioned that the vegetation and its phenology in the proliferation area might have a bearing 10 in the species life cycle (Muralirangan et al. 1997). Chapman & Sword (1997) indicate that the use 11 12 plants for food, shelter or as a roost. There are many references for orthopterans concerning it and, 13 especially for Pamphagidae, there are two clear examples in Acrostira euphorbiae (López et al. 2007) and 14 15 Prionotropis rhodanica (Foucart & Lecoq 1996). 16 Acinipe segurensis has been always related to presence of Rosmarinus officinalis in its habitat (García & 17 Presa 1985; Gómez Ladrón de Guevara et al. 1992; Llorente & Presa 1997; Hernández et al. 1998; Gómez 18 For Peer Review Only 19 Ladrón de Guevara et al. 2009, among others). This plant serves it as a refuge, perch and food. Although 20 A. segurensis is considered a polyphagous species (Gómez Ladrón de Guevara et al. 2009), as all 21 22 (Chapman 1990), it has been always observed in nature feeding on rosemary. Even, 23 sometimes a decline of its populations has been observed after collecting the rosemary for essential oils 24 25 extraction (Gómez Ladrón de Guevara et al. 1992). In studies of food preference (unpublished data), all the 26 stages except nymph I prefer the rosemary. Thus, it could be considered that its diet is governed by the 27 abundance of the host plant as occurs in other species following Chapman (1990). It also could be 28 29 considered as a polyphagous species related to a concrete plant due to different ecological reasons 30 (Chapman & Sword 1997). 31 32 33 Conclusion 34 35 The results provided here contribute to enlarge the knowledge on the biology of A. segurensis. The 36 identification of the different larval stages can facilitate control strategies when needed. Nevertheless, the 37 38 possible causes of the peculiarities of its biological cycle remain unclear. Maybe such features can be due 39 to a set of closely linked phenomena, as already suggested by Guendouz-Benrima et al. (2011). 40 41 42 Acknowledgments 43 Authors are grateful to Dr. Juan Antonio Delgado for his drawings and to Dr. Nicolás Ubero for his technical support. 44 45 46 References 47 Aiouaz M, Boufersaqui A. 1973. Cycle biologique et croissance morphometrique de Pamphagus elephas (L.). Bulletin 48 de la Société d'histoire naturelle de l'Afrique du Nord. 64(1-2):39-50. 49 50 Boudegzdame B. 1980. Particularités du développement d’Ocneridia volxemi Bol. Pamphagidae d’Afrique du Nord. 51 Comparaisons avec d’autres Acridiens. Problèmes de déplacement chez les Acridiens : réalisations et conséquences. 52 Thèse de Doctorat. Univ. Pierre et Marie Curie, Paris 6. 53 54 Bounechada M & Doumandji S, 2003. Research on Ocneridia volxemi Bol. (Pamphagidae, Orthoptera) in Setifian high 55 plains (North-Eastern of Algeria). Eight Arab Congress of Plant Protection. El-Beida, Libya. p.24. 56 Bounechada M, Doumandji SE, Çiplak B. 2006. Bioecology of the Orthoptera species of the Setifian Plateau, North- 57 East Argelia. Turkish Journal of Zoology. 30:245-253. 58 59 Chapman RF. 1990. Food selection. In: Chapman RF, Joern A editors. Biology of Grasshoppers. Canada: John Wiley 60 & Sons Inc.; p. 39-72.

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1 2 3 Chapman RF, Sword GA. 1997. Polyphagy in the Acridomorpha. In: Gangwere SK, Muralirangan MC, Muralirangan 4 M editors. The bionomics of Grasshoppers. Wallingford: CAB International; p. 183-195. 5 6 Descamps M, Mounassif M. 1972. Le complexe Orchamus, Paracinipe, Acinipe et Pamphagus. Acrida. 1:247-303. 7 Elamin AEH, Abdalla MA, El Naim AM. 2014. The biology of senegalese (Oedaleus senegalensis, 8 Krauss, 1887) (Orthoptera: Acrididae). International Journal of Advances in Life Science and Technology. 1(1):6-15. 9 Foucart A, Lecoq M. 1996. Biologie et dynamique de Prionotropis hystrix rhodanica Uvarov, 1923, dans la plaine de 10 11 la Crau(France) (Orthoptera, Pamphagidae). Bulletin de la Société entomologique de France. 101(1):75-87. 12 García MD, Gómez R, Clemente ME, Presa JJ. 2014. Sound producción in the genus Acinipe Rambur, 1838 13 (Orthoptera: Pamphaginae). Italian Journal of Zoology. 81(2):264-270. 14 15 García MD, Presa JJ. 1985. Estudio faunístico y taxonómico de los Caelifera (Orth., Insecta) de Sierra Espuña (Murcia, 16 SE España). Anales de Biología (Biología 1). 3:55-79. 17 Gómez R, Pavón Benito J, Presa JJ. 2010. Estudio de la evolución de una explosión poblacional de Acinipe segurensis 18 For Peer Review Only (Bolivar, 1908) (Orthoptera, Pamphagidae) en la Península Ibérica. Boletín de la Asociación española de Entomología. 19 20 34(1-2):29-37. 21 Gómez Ladrón de Guevara R, Pavón Benito J, Presa JJ. 2009. Outbreak of Acinipe deceptoria (Bolívar, 1878) and 22 Acinipe segurensis (Bolívar, 1908) (Orthoptera: Pamphagidae) in Castilla-La Mancha (Iberian Peninsula). Anales de 23 24 Biología. 31:33-35. 25 Gómez Ladrón de Guevara R, Presa Asensio JJ, García García MD. 1992. Estudio faunístico y ecológico de los 26 Caelifera (Orthoptera, Insecta) de la sierra del Taibilla (Albacete). Colección Ciencia y Técnica. Albacete: Universidad 27 28 de Castilla-La Mancha. 29 Guendouz-Benrima A, Doumandji Mitiche B, Petit D. 2011. Effects of weak climatic variations on assemblages and 30 life cycles of Orthoptera in North Algeria. Journal of Arid Environments. 75:416-423. 31 Hernández A, Clemente ME, García MD, Presa JJ. 1998. Inventario y dinámica poblacional de los ortopteroides 32 33 (Orthoptera, Blattoptera, Mantodea y Phasmoptera) del parque natural del “Carrascal de la Font Roja” (Alicante, E. 34 España). Zoologica baetica. 9:185-204. 35 Hernández-Teixidor D, López H, Nogales M, Emerson BC, Juan C, Oromí P. 2014. Genetic, morphological, and dietary 36 37 changes associated with novel habitat colonisation in the Canary Island endemic grasshopper Acrostira bellamyi. 38 Ecological Entomology. 39:703-715. 39 Joern A, Gaines SB. 1990. Population dynamics and regulation in Grasshoppers. In: Chapman RF, Joern A editors. 40 Biology of Grasshoppers. Canada: John Wiley & Sons Inc.; p.415-482. 41 42 Korsakoff MN. 1941. Contribution à l'etude des Pamphaginae de l'Afrique du Nord. Bulletin de la Société d’histoire 43 naturelle de l'Afrique du Nord. 32:352-369. 44 Llorente V. 1990. Estudio del comportamiento y desarrollo postembrionario de Acinipe hesperica hesperica Rambur, 45 46 1838, en cautividad (Orthoptera: Pamphagidae). Boletín de Sanidad vegetal. Plagas (Fuera de serie). 20:189-207. 47 Llorente V, García MD, Presa JJ. 1995. Datos sobre el comportamiento de Eumigus punctatus templadoi Llorente & 48 Presa 1986 (Orthoptera, Pamphagidae). Zoologica baetica. 6:23-32. 49 50 Llorente V, Presa JJ. 1997. Los Pamphagidae de la Península Ibérica (Insecta: Orthoptera: Caelifera). Murcia: 51 Servicio de Publicaciones, Universidad de Murcia. 52 López H, Nogales M, Morales E, Oromí P. 2007. Habitat use and phenology of the large insular endemic grasshopper 53 Acrostira euphorbiae (Orthoptera: Pamphagidae). Bulletin of Entomological Research. 97:117-127. 54 55 Massa B. 1990. Due nuove specie di Pamphagus Thunberg dell´Algeria e Marocco (Orthoptera, Pamphagidae), 56 Frustula Entomologica (N.S.). 13(26):199-212. 57 Massa B, Cusimano G. 1979. Nota sulla biología e l´accrescimento di Pamphagus marmoratus Burm. e P. sardeus 58 59 (Herrich-Schaeffer). (Insecta Orthoptera). Il Naturalista Siciliano. (4)3(1-2):27-38. 60

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1 2 3 Massa B, Fontana P, Buzzetti FM, Kleukers R, Odé B. 2012. Fauna d´Italia. Orthoptera. Milano: Calderini-Edizione 4 Calderini de Il Sole. 5 6 Massa B, LoVerde G. 1990. Ciclo biologico delle specie del genere Pamphagus Thunberg, 1815 (Orthoptera, 7 Pamphagidae). Frustula Entomologica (N.S.). 13(26):213-224. 8 Mendizábal M. 1948. Una plaga nueva. Cuadernos de Orientación. 1:11-13. 9 Muralirangan MC, Muralirangan M, Partho PD. 1997. Feeding behaviour and host selection strategies in Acridids. In: 10 11 Gangwere SK, Muralirangan MC, Muralirangan M editors. Bionomics of the Orthopteroids. Wallingford: CAB 12 International; p. 163-182. 13 Petit D. 2014. Climatic changes in Algeria and responses from acridian insects. Revue Agrobiologia. 6:5-12. 14 15 Schädler M, Witsack W. 1999. Variation of postembryonic development time and number instars on a small spatial 16 scale in Central European grasshoppers (Caelifera: Acrididae). Entomologia Generalis. 24(2):125-135. 17 Schultner E, Blanchet E, Pagés C, Lehmann GUC, Lecoq M. 2012. Development, reproductive capacity and diet of the 18 For Peer Review Only Mediterranean grasshopper Arcyptera brevipennis vicheti Harz 1975 (Orthoptera: Caelifera: Acrididae: 19 20 Gomphocerinae). Annales de la Société entomologique de France (N.S.). 48(3-4):299-307. 21 Telfer MG, Hassal M. 1999. Ecotypic differentiation in the grasshopper Chorthippus brunneus: life history varies in 22 relation to climate. Oecologia. 121:245-254. 23 24 Uvarov, B. 1967. Hibernation of active stages of Acridoidea in temperate climates. Atti Accademia Gioenia di Scienze 25 Naturali Catania. 18:175-189. 26 Uvarov, B. 1977. Grasshoppers and Locusts II. A Handbook of General Acridology, Vol.2. London: Centre for 27 28 Overseas Pest Research. 29 30 Figure 1. Acinipe segurensis, male nymph. A–C, Stage I: A, antenna; B, meso- and metanotum in lateral view; C, 31 external genitalia from below. D–F, Stage II: D, antenna; E, meso- and metanotum in lateral view; F, external genitalia 32 from below. G–I, Stage III: G, antenna; H, meso- and metanotum in lateral view; I, external genitalia from below. J– 33 L, Stage IV: J, antenna; K, meso- and metanotum in lateral view; L, external genitalia from below. Legend: E: epiproct; 34 MsW: mesothoracic wing rudiment; MtW: metathoracic wing rudiment; P: paraproct; SG: subgenital plate; WR: wings 35 rudiments. 36 Figure 2. Acinipe segurensis, female nymph. A–C, Stage I: A, antenna; B, meso- and metanotum in lateral view; C, 37 external genitalia from below. D–F, Stage II: D, antenna; E, meso- and metanotum in lateral view; F, external genitalia 38 from below. G–I, Stage III: G, antenna; H, meso- and metanotum in lateral view; I, external genitalia from below. J– 39 L, Stage IV: J, antenna; K, meso- and metanotum in lateral view; L, external genitalia from below. M–O, Stage V: M, 40 antenna; N, meso- and metanotum in lateral view; O, external genitalia from below. Legend: E: epiproct; IV: inner 41 ovipositor valve; LV: lower ovipositor valve; MsW: mesothoracic wing rudiment; MtW: metathoracic wing rudiment; P: paraproct; SG: subgenital plate; UV: upper ovipositor valve; WR: wings rudiments. 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

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1 2 3 Table 1. Length Duration of the nymphal stages of Acinipe segurensis. N: number of individuals studied. 4 Stage length duration (in days) 5 Total 6 Sex N I II III IV V development 7 duration 8 Mean ± SD 10.23 ± 2.05 10.62 ± 2.52 8.37 ± 2.09 7.33 ± 1.91 - 36.56 ± 3.73 9 Male 18 Minimum 8 6 6 6 - 29 10 Maximum 14 15 13 12 - 44 11 Mean ± SD 9.10 ± 1.67 10.76 ± 2.43 8.32 ± 2.50 9.28 ± 1.90 7.88 ± 1.62 45.12 ± 3.46 12 Female 17 Minimum 7 8 4 7 6 38 Maximum 12 16 14 12 11 53 13 14 15 16 17 18 For Peer Review Only 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

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1 2 3 Table 2. Data available for number of nymphal stages, diapause stage and length of intermoult periods in different 4 Pamphagidae species. 5 6 7 Intermoult Number of stages Diapause 8 Species period Reference 9 Male Female Egg Nymph (in days) 10 Acrostira euphorbiae 4 6 X - López et al. (2007) 11 Acinipe hesperica 7 7 X 12-35 Llorente (1990) 12 Acinipe segurensis 4 5 X 4-16 This paper 13 Euryparyphes sitifensis 5 6 X 18-32 Korsakoff (1941) Ocneridia nigropunctata 5 5-6 X - Boudegzdame (1980) 14 Ocneridia volxemii 5 5-6 X - Boudegzdame (1980) 15 Pamphagus elephas 7 7 X 9-15 Aiouaz & Bonfersaqui (1973) 16 Pamphagus sp. 7 7 X 15-20 Massa & LoVerde (1990) 17 18 For Peer Review Only 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

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1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 For Peer Review Only 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 Figure 1. Acinipe segurensis, male nymph. A–C, Stage I: A, antenna; B, meso- and metanotum in lateral 44 view; C, external genitalia from below. D–F, Stage II: D, antenna; E, meso- and metanotum in lateral view; 45 F, external genitalia from below. G–I, Stage III: G, antenna; H, meso- and metanotum in lateral view; I, 46 external genitalia from below. J–L, Stage IV: J, antenna; K, meso- and metanotum in lateral view; L, 47 external genitalia from below. Legend: E: epiproct; MsW: mesothoracic wing rudiment; MtW: metathoracic wing rudiment; P: paraproct; SG: subgenital plate; WR: wings rudiments. 48 49 170x194mm (300 x 300 DPI) 50 51 52 53 54 55 56 57 58 59 60 URL: https://mc.manuscriptcentral.com/tase E-mail: [email protected] Page 13 of 13 Annales de la Société Entomologique de France

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 For Peer Review Only 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 Figure 2. Acinipe segurensis, female nymph. A–C, Stage I: A, antenna; B, meso- and metanotum in lateral 40 view; C, external genitalia from below. D–F, Stage II: D, antenna; E, meso- and metanotum in lateral view; 41 F, external genitalia from below. G–I, Stage III: G, antenna; H, meso- and metanotum in lateral view; I, 42 external genitalia from below. J–L, Stage IV: J, antenna; K, meso- and metanotum in lateral view; L, 43 external genitalia from below. M–O, Stage V: M, antenna; N, meso- and metanotum in lateral view; O, 44 external genitalia from below. Legend: E: epiproct; IV: inner ovipositor valve; LV: lower ovipositor valve; MsW: mesothoracic wing rudiment; MtW: metathoracic wing rudiment; P: paraproct; SG: subgenital plate; 45 UV: upper ovipositor valve; WR: wings rudiments. 46 47 170x173mm (300 x 300 DPI) 48 49 50 51 52 53 54 55 56 57 58 59 60 URL: https://mc.manuscriptcentral.com/tase E-mail: [email protected]