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Revista Brasileira de Entomologia

Print version ISSN 0085-5626On-line version ISSN 1806-9665

Rev. Bras. entomol. vol.60 no.1 São Paulo Jan./Mar. 2016

http://dx.doi.org/10.1016/j.rbe.2015.11.012 

Systematics, Morphology and Biogeography

Description of immature stages of Hoplia mexicana Harold and H. squamifera Burmeister (Coleoptera, Melolonthidae, Hopliinae)

Miguel Ángel Moróna  * 

Andrés Ramírez-Ponceb 

Concepción Ramírez-Salinasc 

Hortensia Carrillo-Ruizd 

aRed de Biodiversidad y Sistemática, Instituto de Ecología, Xalapa, Mexico

bLaboratorio de Biología Evolutiva, Centro Tlaxcala de Biología de la Conducta, Universidad Autónoma de Tlaxcala, Tlaxcala, Mexico

cEl Colegio de la Frontera Sur (ECOSUR), San Cristóbal de Las Casas, Chiapas, Mexico

dLaboratorio de Entomología, Escuela de Biología, Benemérita Universidad Autónoma de Puebla, Puebla, Mexico

ABSTRACT

Third stage larvae and pupae are described based on specimens collected in Mexico: Oaxaca (Cerro Zempoaltepetl), and Chiapas (Amatenango), respectively. Pupal characters are described for the first time for American Hopliinae. Habitus images and figures of diagnostic characters as well as comments on the differences between these larvae and those of Hoplia callipyge LeConte, 1856 and H. equina LeConte, 1880, the only Hopliinae larvae previously known in New World, are also included.

Keywords: Biology; Morphology; Pupae; Taxonomy; White grubs

Introduction

The immature stages of world Hopliinae are poorly known. Partial descriptions exist for the third instar larvae of the North American species Hoplia callipyge LeConte, 1856 (= H. oregona LeConte, 1856; = H. cazieri Boyer, 1940) and H. equina LeConte (Ritcher, 1949). Additionally, there are larval descriptions for some Russian species of the genus Hoplia Illiger, 1803 and the central European H. philanthus (Fuessly, 1775) (Medvedev, 1952; Hůrka and Bílý, 1966). Micó (2001) redescribed the larva of H. philanthus and described that of H. chlorophana Erichson, 1848, based on specimens from Spain, both with detailed illustrations. Ansari et al. (2006, 2008) detailed the life cycle of H. philanthus and commented about the importance and biological regulation of this turf pest.

Larvae of North American species of Hoplia may be characterized as follows: head without stemmata; labrum symmetrical; maxillary stridulatory area with row of 9–11 short teeth with anteriorly directed points; lacinia with longitudinal row of 3 unci, distal 2 unci fused basally, subapical uncus much smaller; epipharynx with plegmatia, plegmata quite short; proplegmatia present or absent; epizygum absent; haptomerum with single helus; dexiophoba and laeophoba absent; haptolachus without microsensilla; spiracles of abdominal segments 1–3 similar in size, spiracles of segments 4–8 much smaller; anal opening Y-shaped; raster consisting of subtriangular teges of 30–60 fairly long hamate setae with curved tips; claws of fore legs large and falcate, claws of middle legs much reduced in size, claws of hind legs minute or absent (Ritcher, 1966). Larvae of European species of Hoplia share all of the above cited characters, except: maxillary stridulatory area with row of 12–14 short teeth with anteriorly directed points; lacinia with subapical uncus large; epipharynx without proplegmatia; spiracles of abdominal segments 4–6 diminutive (Micó, 2001).

During recent years, we had the opportunity to rear many scarab larvae collected from forest soil, grasslands and corn fields of southeastern Mexico, and some of them belong to species of Hoplia. This material allowed us to describe in the present paper the third instar larvae for H. mexicanaHarold, 1869 and H. squamiferaBurmeister, 1844, for which the immature stages were unknown. We also describe the pupae of these two species, a life stage that was unknown for any New World hopliine scarab.

Material and methods

Throughout the descriptions and discussions, we follow terminology employed by Ritcher (1966) and Morón (1986). Drawings of diagnostic structures were made using a Leica stereomicroscope associated with a camera lucida at 0.8–5.0× magnification. Measurements were taken using an ocular micrometer (Leica microsystems, Germany). Voucher specimens were deposited at Colección proyecto Diversidad en Sistemas de Cultivos, El Colegio de la Frontera Sur (ECOSUR), and Colección Entomológica, Instituto de Ecología, A. C. Xalapa, México (IEXA).

Taxonomy

Descriptions

Hoplia mexicanaHarold, 1869

Third instar (Figs. 111 and 13). Description. Head (Fig. 2). Maximum width of head capsule: 1.8–2.0 mm. Surface of cranium smooth, with scattered minute punctures, pale yellowish. Frontal and epicranial sutures hidden. Frons with 2 exterior frontal setae, 3–4 posterior frontal setae, 1 anterior frontal seta, 1 anterior angle seta, 3 dorsoepicranial setae, 8–9 epicranial setae on each side and 7–9 setae behind each antennal support. Clypeus with 2 central setae and 4 lateral seta on each side. Labrum nearly symmetrical with rounded lateral margins irregularly bordered, anterior margin projected forward with irregular border, 6–7 posterior setae, 1 central seta and 3–4 lateral setae on each side. Stemmata absent. Epipharynx (Fig. 5) 1.0–1.1 mm wide, 0.8–0.9 mm long, epizygum absent and zygum as a irregular, ovate, reddish yellow plate. Haptomerum weakly raised, with 4 heli; each plegmatia formed by 8–10 short plegmata; proplegmatia absent. Each acanthoparia with 10–12 spinose setae. Dexiophoba and laeophoba absent. Dexiotorma narrowed, slightly sinuose. Laeotorma elongate and narrowed, with sclerotized plate unciform, raised. Sense cone short. Crepis weakly defined. Left chaetoparia with 28–30 spinose and medium size setae mixed. Right chaetoparia with 30–36 short, stout setae. Mandibles (Figs. 3 and 4) without ventral stridulatory area; scissorial area in both mandibles without distal blade. Right mandible with 1 small preapical tooth, inner margin simply curved, and distal lobe (M1) of molar area scarcely developed. Calx short. Left mandible with 1 small preapical tooth, inner margin simply curved, brustia moderately setose. Acia absent. Maxillae (Figs. 69). Mala with 1 uncus on apex of galea, 3 unci surrounded by 3–4 stout heli on apex of lacinia; stridulatory area with 8 small teeth with anteriorly directed points. Hypopharyngeal sclerome (Fig. 10) asymmetrical with raised and curved projection on the right side. Fourth antennomere elongate, with distal half narrowed, with 1 ovate, dorsal sensory spot on basal half and 2 ventral sensory spots.

Figs. 1–5 Third instar larva of Hoplia mexicana. 1, lateral habitus. 2, head, frontal view. Mandibles, ventral view: 3, left. 4, right. 5, epipharynx. 

Figs. 6–12 Hoplia mexicana. 6–11: third instar larva. Maxillae: dorsal view: 6, left. 7, right. Mesial view: 8, left. 9, right. 10, labium and hypopharynx. 11, raster. 12, MALE pupa, lateral view. 

Figs. 13–16 Hoplia mexicana. 13, Third instar, lateral view. 14–16: male pupa. 14, ventral view. 15, lateral view. 16, dorsal view. 

Thorax. Respiratory plates light yellow, scarcely curved, “C” shaped (Figs. 1 and 13) 0.12–0.14 mm long, 0.10–0.11 mm wide, bulla small, slightly raised, rounded, distance between lobes longer than dorso-ventral diameter of bulla; microscopic holes of respiratory plate elongate-oval in outline and arranged in irregular transverse rows. Lateral sclerome of pronotum not defined. Pro-prescutum with 20–22 long setae regularly distributed; proscutum with 8–9 slender long setae; mesoprescutum with transverse row of 10–12 long setae; mesoscutum with 12–16 setae; mesoscutellum with row of 8–10 slender long setae; metaprescutum with transverse row of 12–16 mixed short and long setae; metascutum with 10–12 setae; metascutellum with transverse row of 10–12 mixed short and long setae (Figs. 1 and 13). Protarsal claws long, narrowed, sharply pointed, with 1 prebasal inner seta and 1 lateral external seta, moderately longer than mesotarsal claws; meso-tarsal claws long, sharply pointed, with pre-basal and lateral setae; metatarsal claw short, rounded, with 2 setae, much shorter than mesotarsal claws. Apical metatarsomere shortened, rounded, with ventral side clearly convex.

Abdomen. Respiratory plates light yellow, slightly curved, “C” shaped; on segments I–IV with similar diameter, 0.12–0.13 mm long, 0.10 mm wide; plates on segments V–VII are slightly smaller, 0.10–0.11 mm length, 0.09 mm width. Plate on segment VIII is smaller than preceding. Dorsa of abdominal segments I–VI each with dense vestiture of yellow stout, short setae; dorsa of segments VII–IX with transverse rows of 20–28 slender, short setae. Venter of abdominal segments I–VIII with transverse rows of 14–18 slender, long setae; venter of segment IX with transverse rows of 12–16 mixed short and long setae.

Raster (Fig. 11) with each palidia formed by 9–11 pali, convergent toward basal and distal extremes, septula wide, oval; tegilla with 20–26 short, stout setae; campus with 14–18 slender, short setae; barbula much more densely setose. Dorsal anal lip with dense vestiture of short setae. Ventral anal lip with scattered short setae toward sides and distal border narrowly notched at middle. Anal slit “Y” shaped. Approximate dorsal body length 16–17 mm.

Description: body length 7.5–7.8 mm. Widest width 4.4–4.5 mm. Head. Surface glabrous, strongly deflexed; frons convex with two rounded prominences; clypeus widely concave on the center; labrum, mandibles, maxillae and palps discernible; antennal theca briefly expanded, stout with apex rounded; eyes small (Fig. 14). Thorax: surface glabrous. Pronotum convex, surface slightly irregular, anterior angles prominent, posterior angles rounded. Meso- and metanotum well-differentiated. Elytral and posterior wing thecae closely appressed, curved ventrally around the body; elytral thecae with irregular depressions and large, prominent, humeral tubercles (Figs. 12 and 15); thecae of the wings slightly longer than elytral thecae. Protibiae with apical and preapical tubercles clearly developed. Meso and metatibiae with apical tubercle. Abdomen: segments I–VI clearly wider and shorter than the distal segments VII–VIII, without dioneiform organs, but segments II–IV with pairs of prominent tubercles and segment V with increased posterior border (Figs. 12 and 1516). Pleural lobes rounded. Spiracle I elongate, with fine peritreme and covered by wing thecae; spiracles II–IV ovate and high, prominent, with narrow sclerotized peritreme; spiracles V–VIII closed. Sutures between segments VIII and X not complete, partially fused. Last segment slightly pruinose, without urogomphi.

Last abdominal segment of male with large dorsal and lateral rounded prominences, and genital ampulla ventrally exposed (Figs. 12 and 1416); female without such prominences at the apex of abdomen.

Specimens examined. Four third instar larvae, four pupae and two exuviae of third instar larvae reared to adults, collected at Mexico: Oaxaca: Santa María Tlahuitoltepec municipality, Cerro Zempoaltepetl, 2400 m, 8-VI-2010, A. Ramírez col. (IEXA).

Comments. The third instar larvae of H. mexicana resemble those of H. callipyge and H. equina, but H. mexicana has 4 heli on haptomerum, and palidia with well-defined septula. Hoplia callipyge and H. equina each have1 helus on the haptomerum and only subtriangular teges of long hamate setae with curved tips. The dense setiferous vestiture on the dorsum of abdominal segments I–VI and the sides of the last segment, aid in distinguishing H. mexicana from the known larvae of other Mexican melolonthine scarabs. Projections on the humeral area of the elytra and the middle of the abdominal segments of the pupae of both sexes may act as auxiliary supports during pupal development. These projections possibly aid in regulating humidity near the body wall. This type of structure is also observed in pupae of some Scarabaeinae (Edmonds and Halffter, 1978), and Ceratocanthinae (Morón and Arce, 2003).

Biology. Hoplia mexicana is known only from the northern mountains of the Mexican state of Oaxaca, at localities with elevations between 2300 and 2500 m. Larvae have been collected in rich organic soil of oak and coniferous forest. Adults are rarely attracted to electric lights during summer, and their host plants are unknown.

Hoplia squamifera Burmeister, 1844

Third instar (Figs. 1724). Description. Head (Fig. 18). Maximum width of head capsule: 2.1–2.4 mm. Surface of cranium smooth, with scattered minute punctures, pale yellowish. Frontal and epicranial sutures hidden. Frons with 2 exterior frontal setae, 1 posterior frontal seta, anterior frontal seta absent, 1 anterior angle seta, 3–4 dorsoepicranial, 14–18 epicranial setae on each side and 6–8 setae behind each antennal support. Clypeus with 2 central setae and 4 lateral setae on each side. Labrum nearly symmetrical with rounded lateral margins irregularly bordered, anterior margin projected forward with irregular border, basal transverse keel with 5 posterior setae, 1 anterior-central seta and 5–6 lateral setae on each side. Stemmata absent. Epipharynx (Fig. 21) 1.6–1.9 mm wide, 1.0–0.2 mm long. Epizygum absent and zygum as irregular, ovate, reddish yellow plate. Haptomerum weakly raised, with 4 heli; each plegmatia formed by 9–10 short plegmata; proplegmatia absent. Each acanthoparia with 9–10 spinose setae. Dexiophoba and laeophoba absent. Dexiotorma narrowed, slightly curved. Laeotorma elongate and narrowed with sclerotized plate unciform, raised. Sense cone short. Crepis weakly defined. Left chaetoparia with 30–34 spinose and medium size setae mixed. Right chaetoparia with 28–30 short, stout setae. Mandibles (Figs. 19 and 20) without ventral stridulatory area; scissorial area in both mandibles without distal blade. Right mandible with 1 small rounded, preapical tooth, inner margin simply curved, and distal lobe (M1) of molar area scarcely developed. Calx short. Left mandible without preapical tooth, inner margin simply curved, brustia moderately setose. Acia absent. Maxillae (Fig. 23). Mala with 1 uncus on apex of galea, 3 unci surrounded by 3–4 stout heli on apex of lacinia; stridulatory area with 10–11 small teeth with anteriorly directed points. Hypopharyngeal sclerome (Fig. 22) asymmetrical with curved projection on the right side. Fourth antennomere elongate, with distal half narrowed, with 1 ovate, dorsal sensory spot on basal half and 2 ventral sensory spots.

Figs. 17–21 Third instar larva of Hoplia squamifera. 17, lateral habitus. 18, head, frontal view. Mandibles, ventral view: 19, left. 20, right. 21, epipharynx. 

Figs. 22–25 Hoplia squamifera. 22–24: third instar. 22, labium and hypopharynx. 23, left maxilla, dorsal view. 24, raster. 25, female pupa, lateral view. 

Thorax. Respiratory plates light yellow, scarcely curved, “C” shaped (Fig. 17) 0.11–0.15 mm long, 0.10–0.12 mm wide, bulla small, slightly raised, rounded, distance between lobes longer than dorso-ventral diameter of bulla; microscopic holes of respiratory plate elongate-oval in outline and arranged in irregular transverse rows. Lateral sclerome of pronotum not defined. Proprescutum with 14–18 long setae regularly distributed; proscutum with 5–6 slender long setae; mesoprescutum with transverse row of 8–9 long setae; mesoscutum with 10–12 setae; mesoscutellum with row of 6–8 slender long setae; metaprescutum with transverse row of 9–12 mixed short and long setae; metascutum with 8–10 setae; metascutellum with transverse row of 6–8 mixed short and long setae (Fig. 17). Protarsal claws long, narrowed, sharply pointed, with 1 pre-basal inner seta and 1 lateral external seta, moderately longer than mesotarsal claws; mesotarsal claws long, sharply pointed, with pre-basal and lateral setae; metatarsal claw short, rounded, with 2 setae, much shorter than mesotarsal claws. Apical metatarsomere shortened, rounded, with ventral side clearly convex.

Abdomen. Respiratory plates light yellow, slightly curved, “C” shaped; on segments I–IV with similar diameter, 0.13–0.14 mm long, 0.11 mm wide; plates on segments V–VII slightly smaller, 0.11–0.12 mm long, 0.10 mm wide. Respiratory plate on segment VIII smaller than plate on preceding segment. Dorsa of abdominal segments I–VI each with dense vestiture of yellow stout, short setae; dorsa of segments VII–IX with transverse rows of 18–20 slender, short setae. Venter of abdominal segments I–VIII with transverse rows of 10–12 slender, long setae; venter of segment IX with transverse rows of 10–12 mixed short and long setae. Raster (Fig. 24) with each palidia formed by 10–12 pali, convergent toward basal and distal extremes, septula wide, oval; tegilla with 24–30 short, stout setae; campus with 14–16 slender, short setae; barbula densely setose. Dorsal anal lip with dense vestiture of short setae.

Ventral anal lip with scattered short setae at sides and distal border narrowly notched at middle. Anal slit “Y” shaped. Approximate dorsal body length 16–18 mm.

Pupa (Figs. 25 and 26). Description: body length 7.8–8.1 mm. Widest width 4.5–4.6 mm. Head. Surface glabrous, strongly deflexed; frons convex with two rounded prominences; clypeus widely concave on the center; labrum, mandibles, maxillae and palps discernible; antennal theca briefly expanded, stout with apex rounded; eyes small (Fig. 25). Thorax: surface glabrous. Pronotum convex, surface slightly irregular, anterior angles briefly prominent, posterior angles widely rounded. Meso- and metanotum well-differentiated. Elytral and posterior wing thecae closely appressed, curved ventrally around body; elytral thecae with irregular longitudinal striae and large, prominent, semiconical humeral tubercles (Figs. 25 and 26); thecae of the wings slightly longer than elytral thecae. Protibiae with apical and preapical tubercles clearly developed. Meso and metatibiae with apical tubercle. Abdomen: segments I–VI clearly wider and shorter than the distal segments VII–VIII, without dioneiform organs, but segments II–IV with pairs of prominent tubercles and segment V with thicker posterior border (Figs. 25 and 26). Pleural lobes rounded. Spiracle I elongate, with fine peritreme partially covered by wing thecae; spiracles II–IV ovate and high, prominent, with narrow sclerotized peritreme; spiracles V–VIII closed. Sutures between segments VIII and X incomplete, partially fused. Last segment slightly pruinose, without urogomphi. Last abdominal segment of male with dorsal and lateral rounded prominences, and genital ampulla ventrally exposed (Fig. 26); female without such abdominal prominences (Fig. 25).

Fig. 26 Male pupa of Hoplia squamifera, with third instar exuviae on its abdominal apex. 

Specimens examined. Seven third instar larvae, collected at Mexico: Chiapas, Amatenango del Valle municipality, El Madronal, 2400 m, 20-I-1997, corn field, C. Ramírez col. (IEXA). Two pupae and 2 exuviae of third instar larvae reared to adults, with same data, except 24-X-2005 (IEXA). Two third instar larvae: Chiapas, Amatenango del Valle, 28-X-1996, corn field, C. Ramírez; 4 third instar larvae with same data, except 4-XI-1996; 5 third instar larvae 24-IX-2001 (IEXA, ECOSUR).

Comments. The larvae of Hoplia squamifera resemble those of H. mexicana, but lack antero-frontal setae, have 9–10 wide plegmata on each plegmatia, and have wide septula, whereas Hoplia mexicana have 2 antero-frontal setae, 7–8 narrow plegmata on each plegmatia and narrower septula.

Pupae of both Hoplia mexicana, and H. squamifera lack urogomphi and dioneiform organs. This fact is very interesting because, as far as we know, no other scarab group possesses such a combination of characters. For instance, with the exception of Manopus biguttatus Laporte, 1840 (Neita-Moreno et al., 2012), known pupae of Melolonthinae have urogomphi and lack dioneiform organs (Table 1). On the other hand, known pupae of Rutelinae and Dynastinae, lack urogomphi but, in contrast, have dioneiform organs (Morón, 1993). With the combination of these characters, and the unique paired supporting organs in the humeri and tergites, the pupae of Hopliinae are very distinct from other subfamilies of Melolonthidae. Description of the pupae of many other genera of Melolonthidae surely will offer more characters to be tested in future phylogenetic analyses of Scarabaeoidea.

Table 1 Main characters in the pupae of some American genera of Scarabaeoidea. D.O., dioneiform organs; H.P., humeral projections; P.P., pronotal projections; T.P., tergal projections; U, urogomphi. 

Subfamilies Genera P.P. H.P. D.O. T.P. U References
Melolonthinae Phyllophaga Harris, 1827 No No No No Yes Morón (1986)
Polyphylla Harris, 1841 No No No No Yes Morón and Nogueira (2015)
Clavipalpus Laporte,Castelnau, 1832 No No No No Yes Neita-Moreno et al. (2012)
Demodema Blanchard, 1850 No No No No Yes Morón and Salvadori (2006)
Isonychus Mannerheim, 1829 No No No No Yes Neita-Moreno et al. (2012)
Macrodactylus Dejean, 1821 No No No No Yes Ramírez-Salinas et al. (2011)
Manopus Laporte Castelnau, 1840 No No No No No Neita-Moreno et al. (2012)
Hopliinae
Rutelinae
Hoplia Illiger, 1803 No Yes No Yes No Present publication
Anomala Samouelle, 1819 No No Yes No No Micó et al. (2003)
Macraspis MacLeay, 1819 No No Yes No No Morón and Paucar-Cabrera (2003)
ChlorotaBurmeister, 1844 No No Yes No No Jameson and Morón (2001)
Chrysophora LeP. & Serville, 1828 No No Yes No No Pardo-Locarno and Morón (2007)
Leucothyreus MacLeay, 1819 No No Yes No No Pardo-Locarno et al. (2006b)
Dynastinae Ligyrus Burmeister, 1847 No No Yes No No Ramírez-Salinas et al. (2004)
Ancognatha Erichson, 1847 No No Yes No No Ramírez-Salinas et al. (2004)
Coelosis Hope, 1837 No No Yes No No Pardo-Locarno et al. (2006a)
Golofa Hope, 1837 No No Yes No No Morón (1995b)
Dynastes Kirby, 1825 No No Yes No No Morón (1987)
Aegopsis Burmeister, 1847 No No Yes No No Neita-Moreno et al. (2014)
Cetoniinae Euphoria Burmeister, 1842 No No No No No Ramírez-Salinas et al. (2001)
Hoplopyga J. Thomson, 1880 No No No No No Morón and Arce (2002)
Gymnetis MacLeay, 1819 No No No No No Morón and Arce (2002)
Neoscelis Schoch, 1897 No No No No No Nogueira et al. (2004)
Trichiinae Inca LePeletier & Serville, 1828 No No Yes No No Morón (1983)
Archedinus Morón & Krikken, 1990 Krikken, 1990 No No Yes No No Morón (1995a)
Orphninae Aegidium Westwood, 1846 No No No Yes Yes Morón (1991)
Ceratocanthinae Ceratocanthus White, 1842 Yes Yes No No Yes Morón and Arce (2003)
Aphodiinae Termitodius Wasmann, 1894 No Yes No Yes Yes Reyes-Castillo and Martínez (1979)
Scarabaeinae Phanaeus MacLeay, 1819 Yes No No Yes No Edmonds (1967)
Eurysternus Dalman, 1824 No No No Yes No López-Guerrero and Morón (1994)

Biology. Hoplia squamifera has been recorded from the Mexican mountains of northern Chiapas and Oaxaca states, southern Veracruz state, and in western Guatemala at localities with elevations between 1200 and 2100 m. Larvae have been collected in soil of corn fields in northern Chiapas, Mexico. Adults are frequently attracted to electric lights during spring and summer, but their host plants are unknown.

Acknowledgements

The aid of Adriana E. Castro (ECOSUR) and Susana Guzmán (Instituto de Biología, UNAM, Mexico, D.F.) during field and technical work is here recognized. The suggestions of two anonymous reviewers were very useful in improving the final version of the manuscript. We thank Bruce Gill (Ottawa, Canada) for his friendly assistance with the English language. This paper was supported in part by the research line “Coleópteros Lamelicornios de América Latina” Instituto de Ecología, A.C. Xalapa, Mexico (# 2004010011).

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Received: April 10, 2015; Accepted: November 09, 2015

* Corresponding author. E-mail:miguel.moron@inecol.mx (M.Á. Morón).

Conflicts of interest

The authors declare no conflicts of interest.

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