Introduction
⌅During periodic fauna monitoring surveys in the Abies pinsapo (commonly known as pinsapos) forests in the Ronda mountains, signs of dryness on the branches, stems and leaves of several pinsapo trees were found. After close examination, feeding injuries on the fir needles were evident. The damage had been made by phytophagous beetles of the family Chrysomelidae, generally called leaf beetles, which were found moving and mating among the needles. Chrysomelids are phytophagous beetles that feed on roots, stems, leaves and flowers (Jolivet, 1987Jolivet P, 1987. Aperçu de la sélection trophique chez les galerucinae. Étude par genre (Coleoptera Chrysomelidae). Bull Annls Soc R Belge Ent 123: 283-307.).
Abies pinsapo Boissier is a conifer which is endemic to the mountains of south-western Spain. It occupies some 1250 ha on the north and north-western slopes in the Natural Parks of Sierra de Grazalema (Cádiz), Sierra Bermeja and Sierra de las Nieves National Park (Málaga). Its range is from 1000 to 1800 m above sea level. The height of this species can reach up to 30 meters. Another fir species in northern Morocco, Abies maroccana, is considered to be a subspecies of the nominotypical species (Amaral Franco, 1986Amaral Franco J do, 1986. Pinaceae. In: Flora ibérica, 1; Castroviejo S et al. (eds.). pp: 165-167. Real Jardín Botánico, CSIC, Madrid. http://www.floraiberica.org/ [20/06/2023].; Herrera et al., 2001Herrera J, Arista M, Talavera S, 2001. Abies pinsapo. In: Libro Rojo de la flora silvestre amenazada de Andalucía. Tomo I: Especies en peligro de extinción. pp. 34-38. Consejería de Medio Ambiente, Junta de Andalucía.).
The Andalusian fir trees represent an exceptional case of a temperate forest in a Mediterranean climate (Arista, 1995Arista M, 1995. The structure and dynamics of an Abies pinsapo forest in southern Spain. For Ecol Manag 74 (1-3): 81-89. https://doi.org/10.1016/0378-1127(94)03507-S; Navarro Cerrillo et al., 2006Navarro Cerrillo RM, Lara Fernández A, Blanco Oyonarte P, Calzado Martínez C, López Quintanilla J, Fernández Cancio A, et al., 2006. Aproximación a la definición del hábitat fisiográfico del Abies pinsapo Boiss. en Andalucía. Invest Agr: Sist Recur For (Fuera de Serie): 137-152. https://doi.org/10.5424/srf/200615S1-00988). This Spanish fir is currently in danger of extinction. Among the threat factors is habitat fragmentation, genetic homogenization, and global and climate change. The Andalusian fir forms monospecific woodlands or forests mixed with Quercus rotundifolia and Q. faginea, on calcareous or serpentine soils (Amaral Franco, 1986Amaral Franco J do, 1986. Pinaceae. In: Flora ibérica, 1; Castroviejo S et al. (eds.). pp: 165-167. Real Jardín Botánico, CSIC, Madrid. http://www.floraiberica.org/ [20/06/2023].). An in-depth description about the pinsapo species and woodlands is found in López-Quintanilla (2013)López Quintanilla J (ed.), 2013. Los pinsapares en Andalucía (Abies pinsapo Boiss.): conservación y sostenibilidad en el siglo XXI. Junta de Andalucía, Sevilla, 574 pp..
In this paper we report the first identified defoliating agent of A. pinsapo needles, which belongs to the phytophagous family Chrysomelidae, give its recognition characteristics and describe the injury that produces on the needles and branches.
Material and methods
⌅The study took place in the Sierra de Grazalema Natural Park (Cádiz), Sierra Bermeja Natural Park and Sierra de las Nieves National Park (Málaga), in Andalucía, southern Spain (Fig. 1).
Sampling was carried out at least once per year from 2001 to 2022. The sites wherein the injuring beetles were detected were monitored 2-3 per year, amounting to 40 visits in total.
Body length of the beetles was measured with the ocular grid of a Nikon SMZ-10 stereoscopic microscope at a magnification of 10X. Photographs of the habitus and genitalia were taken with a Leica S9I stereo microscope and a Canon EOS 550D photographic camera attached to a Nikon Alphaphot-2 YS2 microscope, respectively. Zerene Stacker® was used for stacking the photographs. Photographs of live beetles and trees were taken with a Fujifilm FinePix HS10.
The beetles were identified using the keys provided by Laboissière (1912)Laboissière V, 1912. Revision des Galerucini d’Europe et pays limitrophes (suite). Annls Ass Nat Levallois-Perret 18: 13-55., Warchałowski (2010)Warchałowski A, 2010. The Palaearctic Chrysomelidae. Identification keys. 2 vols. Natura Optima Dux Foundation. Warszawa. 1212 pp. and Vela (2018)Vela JM, 2018. On the identity of Calomicrus fallax (Joannis, 1865) with description of a new, widespread species of Calomicrus from Spain and Portugal and comments on the Iberian species (Coleoptera, Chrysomelidae, Galerucinae). Graellsia 74(2): e074. https://doi.org/10.3989/graellsia.2018.v74.204.
Results and discussion
⌅The phytophagous beetles injuring pinsapo needles were identified as Calomicrus foveolatus Rosenhauer, 1856, a beetle of the Chrysomelidae in the subfamily Galerucinae, tribe Luperini. Among Iberian fauna there are five species belonging to the Calomicrus genus: C. circumfusus (Marsham, 1802), C. suturalis (Joannis, 1865), C. sordidus (Kiesenwetter, 1873), C. ibericusVela, 2008Vela JM, 2018. On the identity of Calomicrus fallax (Joannis, 1865) with description of a new, widespread species of Calomicrus from Spain and Portugal and comments on the Iberian species (Coleoptera, Chrysomelidae, Galerucinae). Graellsia 74(2): e074. https://doi.org/10.3989/graellsia.2018.v74.204, and C. foveolatus (see Vela, 2018Vela JM, 2018. On the identity of Calomicrus fallax (Joannis, 1865) with description of a new, widespread species of Calomicrus from Spain and Portugal and comments on the Iberian species (Coleoptera, Chrysomelidae, Galerucinae). Graellsia 74(2): e074. https://doi.org/10.3989/graellsia.2018.v74.204); of these, the last three are endemic to the Iberian Peninsula. Moreover, C. foveolatus was formerly found in the Granada and Málaga provinces, while C. sordidus was recorded in Jaén, Málaga and Cádiz. Thus, these two species are endemic to Andalusia (Vela & Bastazo, 1999Vela JM, Bastazo G, 1999. Ecological and biogeographical aspects of the Andalusian leaf beetles endemisms. In: Advances in Chrysomelidae Biology; Cox ML (ed.). pp. 137-158. Backhuys Publs., Leiden.; Vela, 2018Vela JM, 2018. On the identity of Calomicrus fallax (Joannis, 1865) with description of a new, widespread species of Calomicrus from Spain and Portugal and comments on the Iberian species (Coleoptera, Chrysomelidae, Galerucinae). Graellsia 74(2): e074. https://doi.org/10.3989/graellsia.2018.v74.204).
A short description of C. foveolatus and data on the damage are given below.
Habitus. Medium sized beetle, of 2.67-3.29 mm (males, n=10) and 3.27-3.90 mm (females, n=10). Black teguments (Fig. 2a). Legs, antennae, mandibles, base of the labrum and palps yellow. Antennae and mandibles darker at the apex, with a brownish hue. Tarsomeres III and IV usually brownish. Base of metatarsomere I with a black or dark brown ring. Anterior part of the head, behind the eyes, brown or brown yellowish. Males: central lobe at the apex of the urosternite with a quadrangular depression.
Genitalia. Penis in ventral view truncated at the apex, weakly sinuated, lateral sides convergent to the distal third, after widened slightly to the apex; basal foramen with a very weak medial constriction (Fig. 2b). In lateral view, penis curved in the dorsal region, and straight in the ventral part (Fig. 2c). Spermatheca falciform, with basal ampulla swollen and well differentiated, neck very curved and cornu long; ductus attached to the posterior-superior part of the ampulla (Figs. 2d, 2e).
Distribution. This beetle species was only found in the Granada and Málaga provinces in Andalusia, southern Spain (Vela, 2018Vela JM, 2018. On the identity of Calomicrus fallax (Joannis, 1865) with description of a new, widespread species of Calomicrus from Spain and Portugal and comments on the Iberian species (Coleoptera, Chrysomelidae, Galerucinae). Graellsia 74(2): e074. https://doi.org/10.3989/graellsia.2018.v74.204). However, here it is also reported from the following sites: Almería, Paterna del Río, 29-VI-1975, 1 ♀, leg. M. Daccordi; Almería, Sierra de Gádor, El Marchal de Antón López, 950m, 27-IV-2011, ♀ on Quercus sp., leg. J. Pelikan; Cádiz, Jimena de la Frontera, 500m, 17-V-1998, 1 ♂, 1 ♀, leg. A. Warchałowski (Daccordi´s Collection, Verona, Italy).
Host-plants. In the case of the Galerucinae of tribe Luperini, adults feed on the aerial part of the plant while larvae usually feed on the roots. Little is known about the biology of the larval stage of this tribe (Jolivet, 1987Jolivet P, 1987. Aperçu de la sélection trophique chez les galerucinae. Étude par genre (Coleoptera Chrysomelidae). Bull Annls Soc R Belge Ent 123: 283-307.). The host-plants formerly identified for C. foveolatus adults were Quercus suber, Q. rotundifolia (Vela & Bastazo, 1999Vela JM, Bastazo G, 1999. Ecological and biogeographical aspects of the Andalusian leaf beetles endemisms. In: Advances in Chrysomelidae Biology; Cox ML (ed.). pp. 137-158. Backhuys Publs., Leiden.) and Q. coccifera (Vela, unpublished data) which are all in the Fagaceae family. The feeding record of C. foveolatus on A. pinsapo is a newly identified, extraordinary case of allotrophy from Fagaceae to Pinaceae. The two tree families are widely separated phylogenetically, as the Quercus species are angiosperms and A. pinsapo is a gymnosperm. The early divergent groups of Coleoptera Phytophaga are associated with gymnosperms (cycads and conifers). Such association is considered plesiomorphic within Phytophaga (Farrell, 1998Farrell BD, 1998. ‘’Inordinate Fondness’’ explained: Why are there so many beetles? Science 281: 555-559. https://doi.org/10.1126/science.281.5376.555). The diversity of groups of Phytophaga associated with conifers is scarce compared to those associated with angiosperms (Haddad & McKenna, 2016Haddad S, McKenna DD, 2016. Phylogeny and evolution of the superfamily Chrysomeloidea (Coleoptera: Cucujiformia). Syst Entomol 41: 697-716. https://doi.org/10.1111/syen.12179). Possibly, the affinity for gymnosperms found in some genera and species of Chrysomelidae in the subfamily Galerucinae is a secondary adaptation, because Galerucinae is not a basal group in Phytophaga (Nie et al., 2020Nie RE, Andújar C, Gómez-Rodríguez C, Bai M, Xue HJ, Tang M, et al., 2020. The phylogeny of leaf beetles (Chrysomelidae) inferred from mitochondrial genomes. Syst Entomol 45(1): 188-204. https://doi.org/10.1111/syen.12387). Jolivet & Hawskewood (1995)Jolivet P, Hawkeswood TJ, 1995. Host-plants of Chrysomelidae of the world: an essay about the relationships between the leaf-beetles and their food-plants. Backhuys, Leyden, 281 pp. reported several Galerucinae genera such as Arthrotus Motschulsky, 1858, Sphenoraia Clark, 1865, Monolepta Chevrolat, 1836, Atrachya Dejean, 1836, Paleosepharia Laboissière, 1936, and Morphosphaera Baly, 1861, among which one or more species can select gymnosperms as hosts.
A closely related species to C. foveolatus, C. pardoi Codina, 1961Codina Padilla F, 1961. Nota sobre los Luperus marroquíes del subgénero Calomicrus Stephens (Col. Chrysomelidae). Graellsia 19: 69-79., from the Moroccan Rif and Middle Atlas, was originally described on Quercus sp. (Codina, 1961Codina Padilla F, 1961. Nota sobre los Luperus marroquíes del subgénero Calomicrus Stephens (Col. Chrysomelidae). Graellsia 19: 69-79.), although it was later reported to cause damage to Cedrus atlantica (Endl.) Manetti ex Carrière (Mouna, 1986Mouna M, 1986. Luperus (Calomicrus) pardoi Codina (Col. Chrysomelidae), ravageur phytophage à l’état adulte du cèdre (Cedrus atlantica) au Maroc. Bull Inst Sci Rabat 10: 207-208.; Mouna & Avcı, 2016Mouna M, Avcı M, 2016. Cedar forests under threat of new pests. Turk J For 17 (Spec): 71-75. https://doi.org/10.18182/tjf.75899). Calomicrus apicalis Demaison, 1891, spread throughout Turkey and Syria, feeds on Pinus brutia Ten., P. nigra J. F. Arnold, P. sylvestris L. and Cedrus libani A. Rich. (Gök & Duran, 2004Gök A, Duran E, 2004. A survey of the subfamily Galerucinae (Coleoptera: Chrysomelidae) of Isparta Province (Turkey), with two new records. J Ent Res Soc 6(2): 15-24.; Gök & Çilbiroğlu, 2005Gök A, Çilbiroğlu EG, 2005. Studies on the abundance, biology and harmfulness of leaf beetles (Coleoptera: Chrysomelidae) in natural bush vegetation in Isparta, Turkey. J Pest Sci 78: 13-15. https://doi.org/10.1007/s10340-004-0061-6). Moreover, Aytar et al. (2011)Aytar F, Dağdas S, Duran C, 2011. Biology and control of Calomicrus apicalis Demaison, 1891 (Col.: Chrysomelidae), a new pest of Cedrus libani A. Rich. in Turkey. Silva Lusit (especial): 33-40. found it causing significant damage to the C. libani formations in southern Turkey. Another genus closely related to Calomicrus is Euluperus, which contains three Pinus feeding species. Euluperus pinicola, from Central Europe, was reported on Pinus sylvestris, P. nigra and P. mugo Turra (cited as P. montana Mill.) (Laboissière, 1934Laboissière V, 1934. Galerucinae de la faune française. Ann Soc Entomol Fr 103: 1-108. https://doi.org/10.1080/21686351.1934.12280236; Müller, 1953Müller G, 1953. I coleotteri della Venezia Giulia. Catalogo regionato con tabelle dichotomiche per la classificazione delle specie della regione adriática orientale, del Veneto e della pianura padana, Vol II: Coleoptera Phytophaga (Cerambycidae, Chrysomelidae, Bruchidae). Centro Sperimentale Agrario e Forestale (pubblicazione n. 4), Trieste, 685 pp.; Hiller, 1975Hiller E, 1975. Zur Kenntnis des Schwarbraunen Kiefernblattkäfers, Luperus pinicola (Dftsch.) (Col., Chrysomelidae). Z Angew Entomol 79: 398-421. https://doi.org/10.1111/j.1439-0418.1975.tb02363.x). Calomicrus gularis Gredler, 1857 (really belonging to Euluperus genus), known from Austria, France, Italy, Slovenia and Croatia, was cited on Pinus mugo (as P. montana) and P. sylvestris (Müller, 1953Müller G, 1953. I coleotteri della Venezia Giulia. Catalogo regionato con tabelle dichotomiche per la classificazione delle specie della regione adriática orientale, del Veneto e della pianura padana, Vol II: Coleoptera Phytophaga (Cerambycidae, Chrysomelidae, Bruchidae). Centro Sperimentale Agrario e Forestale (pubblicazione n. 4), Trieste, 685 pp.). Finally, Euluperus espanoli (Codina, 1963), a Spanish endemism, is also a pine consuming species, reported on Pinus sylvestris (Vela, 2018Vela JM, 2018. On the identity of Calomicrus fallax (Joannis, 1865) with description of a new, widespread species of Calomicrus from Spain and Portugal and comments on the Iberian species (Coleoptera, Chrysomelidae, Galerucinae). Graellsia 74(2): e074. https://doi.org/10.3989/graellsia.2018.v74.204) and Pinus halepensis Miller, 1768 (Pérez-Onteniente, 2019Pérez-Onteniente A, 2019. Nuevos registros de Calomicrus ibericus Vela, 2018 y Euluperus espanoli (Codina, 1963) (Coleoptera, Chrysomelidae, Galerucinae) en España. Boletín de la SEA 64: 277-278.). Therefore, there is a tendency in several species of Calomicrus and Euluperus to feed on species in the Pinaceae family (Pinus, Cedrus and Abies).
Picard (1936)Picard F, 1936. Sur un cas d’allotrophie chez Galerucella nymphaeae L. (Col. Chrysomelidae). Bull Soc Entomol Fr 41(3): 45-46. https://doi.org/10.3406/bsef.1936.14961, Jolivet (1952)Jolivet P, 1952. Allotrophie et Chrysomélides. Nat Belg 33 (3-4): 53-59. and Jolivet & Petitpierre (1981)Jolivet P, Petitpierre E, 1981. Biology of Chrysomelidae (Coleoptera). Butll Inst Cat Hist Nat 47 (Sec. Zool. 4): 105-138. used the term allotrophy for the cases where a beetle is found to feed on a host-plant completely unrelated to its normally preferred primary host. This is the case of Calomicrus foveolatus. Just as C. pardoi became capable of feeding on Cedrus in Morocco, C. foveolatus changed from Quercus sp. (Fagaceae) to Abies. Furthermore, the other above-mentioned species appear to only feed on Pinaceae. It is difficult to know what causes the feeding shift from Fagaceae to Pinaceae. The shift could be attributed to the lack of resources provided by Quercus, whose growing period has shortened due to water scarcity. Thus, the beetles can benefit from the switch to young branches of Pinaceae.
Field observations of the damage on Andalusian firs
⌅The beetles were observed on A. pinsapo in the Puntal de la Mesa area (318388/4059625 ETRS89-30N) of the Parauta Municipal District, in the Sierra de las Nieves National Park, on 28/05/2011, 8/06/2011, 14-21-27/06/2019, 05/06/2020, and 2-9-11/06/2022. In almost all the observations the beetles were mating or feeding (Figs. 3a, 3b). Voucher specimens were collected on 28/05/2011, 21/06/2019, and 5/06/2020.
On the other hand, defoliation due to C. foveolatus feeding activity (Fig. 3c) was observed in 2007, 2011, 2014, 2015, 2018, 2019, 2020, 2021 and 2022 in the Puntal de la Mesa (Parauta), in 2011 in the Puerto del Cuco (Yunquera) and in 2022 in the Puerto Corona (Tolox), in the Sierra de las Nieves National Park (Málaga province), and in Peñón Grande and Puerto de Las Palomas, in the Sierra de Grazalema Natural Park (Cádiz province) (Fig. 1).
Throughout the period of observations, the largest area of damage due to defoliation was detected in 2019 in the Puntal de la Mesa (Parauta, Nat. Park Sierra de las Nieves), where approximately 8 ha were affected. In every other affected spot, the damaged area was only approximately 0.2 ha.
In medium and small firs, C. foveolatus specimens prefer the upper half of the crown and needles of the distal part of the shoots on branches facing south and southeast. However, when they appeared in larger adult trees, they were located in the branches of the lower third, extending from there to the rest of the tree. This behaviour could indicate a heliophilic preference. They were found feeding on fir needles of new growing shoots, causing partial and superficial gnawing damage on the upper side of the needles, ultimately causing death of the shoots (Fig. 3d).
The A. pinsapo trees are also affected by several other Coleoptera. The most damaging beetle is reported to be the bark beetle Cryphalus numidicus Eichhoff, 1878 (Curculionidae). Anthaxia (Anthaxia) ceballosi Escalera, 1931, Anthaxia (Haplanthaxia) confusa Gory, 1841, Anthaxia (Haplanthaxia) parallela Laporte & Gory, 1839, A. (Melanthaxia) sepulchralis Fabricius, 1801, Bupestris flavoangulata ssp. baetica Verdugo, 2005Verdugo A, 2005. Fauna de Buprestidae de la Península Ibérica y Baleares (Coleoptera). Argania editio, Barcelona, 350 pp., B. haemorrhoidalis Herbst, 1780 (Buprestidae), Ergates faber (Linnaeus, 1761), Hylotrupes bajulus (L., 1758) (Cerambycidae), Orthotomicus erosus (Wollaston, 1857) (cited as Ips), Crypturgus mediterraneus Eichhoff, 1871, Cr. numidicus Ferrari, 1867, Pityophthorus pinsapo Pfeffer, 1982, Rhyncolus elongatus (Gyllenhal, 1827), Brachytemnus porcatus (Germar, 1823) (cited as Rhyncolus), Otiorhynchus jaenensis Stierlin, 1873 (Curculionidae), and Calopus serraticornis (L., 1758) (Oedemeridae) (Barbey, 1996Barbey A, 1996. A través de los bosques de pinsapo de Andalucía. [Reedición de: A travers les fôrets de pinsapo d’Andalousie, 1931]. Consejería de Medio Ambiente, Junta de Andalucía, Sevilla, 143 pp.; Cobos Suárez, 1994Cobos Suárez JM, 1994. Estado fitosanitario de los pinsapares andaluces. In: Gestión y conservación de los pinsapares andaluces; Cueto Álvarez de Sotomayor MC, Sánchez García JM (coords.). pp. 35-40. Asociación Forestal Andaluza, Monografías Forestales Andaluzas nº 1, Cádiz.; Verdugo, 2005Verdugo A, 2005. Fauna de Buprestidae de la Península Ibérica y Baleares (Coleoptera). Argania editio, Barcelona, 350 pp.; Valladares, 2009Valladares A, 2009. Abetales de Abies pinsapo Boiss. In: Bases ecológicas preliminares para la conservación de los tipos de hábitat de interés comunitario en España; Bermejo E, Melado F. (coords.). Dirección General de Medio Natural y Política Forestal, Ministerio de Medio Ambiente y Medio Rural y Marino, 90 pp.) are other beetles that have been recorded on live or dead parts of pinsapo. Of them, Anthaxia (Haplanthaxia) confusa should be verified, because it normally feeds on Cupresaceae (Verdugo, 2005Verdugo A, 2005. Fauna de Buprestidae de la Península Ibérica y Baleares (Coleoptera). Argania editio, Barcelona, 350 pp.). All the reported beetles are xylophagous.
Among these beetles, Pityophtorus pinsapo and Anthaxia ceballosi are endemic to the Baetic Mountains where Abies pinsapo is their only host (Plaza, 1983Plaza E, 1983. Los representantes españoles de las tribus Crypturgini y Pityophthorini (Col., Scolytidae). Eos 59: 223-241., Verdugo, 2005Verdugo A, 2005. Fauna de Buprestidae de la Península Ibérica y Baleares (Coleoptera). Argania editio, Barcelona, 350 pp.). However, the whole of the insect fauna associated with pinsapo is an important part of the biodiversity and contributes to the stability of the system, forming part of the trophic food web that also includes vertebrates (Lieutier et al., 2016Lieutier F, Mendel Z & Faccoli M, 2016. Bark beetles of mediterranean conifers. In: Insects and diseases of mediterranean forest systems; Paine TD, Lieutier F (eds.). pp. 105-197. Springer, Switzerland, 892 pp. https://doi.org/10.1007/978-3-319-24744-1_6).
It is worth noting the absence of damage by defoliating insects on pinsapo until now. C. foveolatus is the first identified defoliating agent of A. pinsapo needles. Monitoring of the beetle populations on pinsapos will be necessary for sustainable management of pinsapo forests.