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Acta zoológica mexicana

versión On-line ISSN 2448-8445versión impresa ISSN 0065-1737

Acta Zool. Mex vol.37  Xalapa  2021  Epub 21-Feb-2022

https://doi.org/10.21829/azm.2021.3712419 

Articles

Comparative aspects of the internal reproductive system of males in species of Melolonthinae, Dynastinae, and Rutelinae (Coleoptera: Scarabaeoidea) from Mexico

Aspectos comparativos del sistema reproductivo interno de los machos en especies de Melolonthinae, Dynastinae y Rutelinae (Coleoptera: Scarabaeoidea) de México

Imelda Martínez M.1  * 
http://orcid.org/0000-0001-9963-668X

Sara L. Rivera-Gasperín2 
http://orcid.org/0000-0001-6478-9694

Hortensia Carrillo-Ruiz3 
http://orcid.org/0000-0003-4247-6114

Miguel A. Morón 

1Red de Ecoetología, Instituto de Ecología A.C., Carretera Antigua a Coatepec No. 351, El Haya, C.P. 91073, Xalapa, Veracruz, México.

2Red de Biodiversidad y Sistemática, Instituto de Ecología A. C., Carretera Antigua a Coatepec No. 351, El Haya, C.P. 91073, Xalapa, Veracruz, México.

3Laboratorio de Entomología, Facultad de Ciencias Biológicas, Benemérita Universidad Autónoma de Puebla, Blvd. Valsequillo y Av. San Claudio, Colonia Jardines de San Manuel, C.P. 72570, Puebla, Puebla, México.


ABSTRACT

The anatomy of the internal male reproductive systems of 12 species of Melolonthinae (Phyllophaga, Chlaenobia, Macrodactylus, Isonychus), six species of Dynastinae (Cyclocephala), and three species of Rutelinae (Paranomala) (Coleoptera, Scarabaeoidea) of Mexico are described. A total of 350 male specimens representing 21 species were collected. From each species, the reproductive systems were obtained by micro-dissection, placed in a liquid fixative, stained, and drawn to scale. The internal genitalia of each species was described and compared among the species examined. The reproductive system of the Melolonthinae species is comprised of two testicles, each with six follicles, two deferent ducts, two accessory glands, two glandular ducts, an ejaculatory duct, and the aedeagus (not described for any of the species examined). The number of testicular follicles per testicle is as reported in different species of other Scarabaeoidea subfamilies. The length of the accessory glands and the ejaculatory duct varies in the species studied. The ejaculatory bulb is present in all of the species of Dynastinae and Rutelinae examined but in only three species of Melolonthinae.

Key words: internal genitalia; comparative data; males; June bugs

RESUMEN

Se describió la anatomía del sistema reproductivo interno de los machos en 12 especies de Melolonthinae (Phyllophaga, Chlaenobia, Macrodactylus, Isonychus), seis de Dynastinae (Cyclocephala) y tres de Rutelinae (Paranomala) (Coleoptera, Scarabaeoidea) de México. Se recolectaron un total de 350 ejemplares machos representantes de 21 especies. De cada especie se obtuvieron los sistemas reproductivos por microdisección y fueron colocados en un líquido fijador, después teñidos y dibujados a escala. Se describió la genitalia interna de cada especie y se comparó entre las especies examinadas. El sistema reproductivo de las especies de Melolonthinae consta de dos testículos cada uno con seis folículos, dos conductos deferentes, dos glándulas accesorias, dos conductos glandulares, un conducto eyaculador y el edeago (no descrito en ninguna especie). El número de folículos testiculares por testículo es igual al conocido en diferentes especies de otras subfamilias de Scarabaeoidea. La longitud de las glándulas accesorias y del conducto eyaculador varían dependiendo de cada especie estudiada. Un bulbo eyaculador está presente sólo en tres especies de Melolonthinae y en todas las especies de Dynastinae y Rutelinae examinadas.

Palabras clave: genitalia interna; datos comparativos; machos; escarabajos de mayo

INTRODUCTION

The species of Scarabaeidae exhibit great morphological and ecological diversity, which is reflected in the anatomy of their reproductive system. However, the anatomy of the male reproductive system in this family has received very little study, except for the aedeagus, which is often used for species identification (Sharp & Muir, 1912). Unfortunately, only some isolated descriptions of the male internal genitalia in representatives of different Scarabaeidae subfamilies are available.

In Melolonthinae, there are morphological descriptions of the male reproductive system for Melolontha melolontha (Linnaeus) (Dufour, 1825; Straus-Dürckheim, 1828; Bordas, 1900), Anoxia villosa (Fabricius) and Hymenoplia strigosa (Illiger) (Bordas, 1900), Phyllophaga sp. (Williams, 1945), Amphimallon majale (Razoumowsky) (Menees, 1963), Costelytra zealandica (White) (Fenemore, 1971; Stringer, 1990), Phyllophaga anxia (LeConte) (Berberet & Helms, 1972), Phyllophaga sanctipauli (Blanchard) (Diefenbach et al., 1998), Prodontria lewisi Broun (Ferreira & McKinlay, 2001), Macrodactylus mexicanus Burmeister (Benítez-Herrera et al., 2015) Hoplia argentea (Poda) (Bordas, 1900), H. subcostata Bates and H. squamifera Burmeister (Carrillo-Ruiz et al., 2008).

In Dynastinae the male reproductive system has been studied for Oryctes nasicornis (Linnaeus) (Straus-Dürckheim, 1828), Oryctes rhinoceros (Linnaeus) (Mathur et al., 1960; Jacob, 1989) and Adoryphorus couloni (Burmeister) (Hardy, 1981).

In Rutelinae it has been studied for Anisoplia agricola (Poda) (Bordas, 1900), Anomala dubia (Scopoli) and Phyllopertha horticola (Linnaeus) (Rittershaus, 1927), Popillia japonica Newman (Williams, 1945; Anderson, 1950), Anomala ausonia Erichson (Lupo, 1947), and Chrysina costata (Blanchard) (Morón, 2010).

Due to the limited knowledge of the internal genitalia of males in Scarabaeidae, here is described and illustrated for 21 Mexican June bug species. The systems of these species are compared with those reported in other published studies, differentiating between some subfamilies of Scarabaeidae and other families of Scarabaeoidea. The external genitalia were not studied because it is well known and used for taxonomic purposes (Sharp & Muir, 1912).

This study is a contribution to the line of research Biología, Sistemática e Importancia de los Coleópteros Lamelicornios en América Latina, established by the late Miguel Ángel Morón several years ago.

MATERIALS AND METHODS

The adults of most of the species studied were collected in May and June over several years, from different places where it was known that they could be found. Beetles were collected manually, at random, mainly near Xalapa City, Veracruz, Mexico. A total of 350 males of the different species were collected. The species were determined by Miguel Angel Morón†.

The species studied were the following:

Melolonthinae. Phyllophaga testaceipennis (Blanchard) (El Sumidero, Xalapa, Veracruz), Phyllophaga (Phytalus) obsoleta (Blanchard) (El Sumidero, Xalapa, Veracruz), Phyllophaga (s. str.) opaca (Moser) (Valle del Carrizo, Ahome, Sinaloa), Phyllophaga (Phytalus) pruinosa (Blanchard) (Coatepec, Veracruz), Phyllophaga (s. str.) ravida (Blanchard) (El Haya, Xalapa, Veracruz), Phyllophaga (s. str.) rugipennis (Schauffus) (Briones, Coatepec, Veracruz), Phyllophaga (s. str.) setifera (Burmeister) (La Higuera, Xalapa, Veracruz), Phyllophaga (s. str.) subrugosa (Moser) (Briones, Coatepec, Veracruz), Phyllophaga (s. str.) tenuipilis (Bates) (Las Ánimas, Xalapa, Veracruz), Chlaenobia latipes Bates (Las Ánimas, Xalapa, Veracruz), Macrodactylus nigripes Bates (Las Vigas, Veracruz) and Isonychus neglectus Moser (Briones, Coatepec, Veracruz).

Dynastinae. Cyclocephala jalapensis Casey (Rancho Guadalupe, Xalapa, Veracruz), Cyclocephala picta Burmeister (Briones, Coatepec, Veracruz), Cyclocephala sexpunctata Castelnau (Briones, Coatepec, Veracruz), Cyclocephala mafaffa Burmeister (Briones, Coatepec, Veracruz), Cyclocephala lunulata Burmeister (Briones, Coatepec, Veracruz), and Cyclocephala weidneri Endrödi (Briones, Coatepec, Veracruz).

Rutelinae. Paranomala marginicollis (Bates) (Briones, Coatepec, Veracruz). Paranomala semicincta (Bates) (Briones, Coatepec, Veracruz), and Paranomala cupricollis (Chevrolat) (Briones, Coatepec, Veracruz).

The suprageneric classification used follows the proposal of Smith (2006). All examined specimens were deposited in the collection of Miguel Ángel Morón, Xalapa, Veracruz, Mexico (MXAL).

For each species two to ten live males were selected and dissected in Ringer’s saline solution to obtain their reproductive system. The complete system from each male was placed and extended in AFATD fixer (96% ethanol-formaldehyde-trichloroacetic acid-dimethylsulfoxide), and later completely stained using the Feulgen light green and chlorazol black staining techniques (Martoja & Martoja, 1967; Gabe, 1968; Carayon, 1969; Martínez, 2002). The internal genitalia of several specimens of each species were initially observed and drawn to scale using a stereomicroscope with a camera lucida (Zeiss® SV11). For each species Chinese ink was used for the line drawings (unpublished techniques, learned by the first author directly from J. Carayon and Dominique Pluot-Sigwalt). The figures were edited into plates using Corel Photo-Paint® software. The descriptions use the terminology of Snodgrass (1935) and Matzuda (1976) for the general morphology of the internal genitalia.

RESULTS

In general terms, the males of these three subfamilies have similar reproductive systems, though there are some differences between them.

Melolonthinae (Fig. 1-12). The male reproductive system of P. testaceipennis (Fig. 1) is typical of all of the Melolonthinae species examined. It consists of two testes, each with six lobed and dorsoventrally flattened testicular follicles, without an outer membrane to group them together. Each testicular follicle has a long and very visible vas efferens, which emerges from the ventral region. The six vas efferens flow into the vas deferens of each testis.

Figures 1-12 Male reproductive system of 12 species of Melolonthinae. 1. Phyllophaga testaceipennis 2. Ph. obsoleta 3. Phy opaca 4. Ph. pruinosa 5. Ph. ravida 6. Ph. rugipennis 7. Ph. setifera 8. Ph. subrugosa 9. Ph. tenuipilis 10. Chlaenobia latipes 11. Macrodactylus nigripes 12. Isonychus neglectus. Only in P. testaceipennis is the complete reproductive system shown, in the other figures only half is shown. (ae= aedeagus, ag= accessory glands, eb= ejaculatory bulb, ed= ejaculatory duct, gd= glandular duct, gr=glandular reservoir, te= testis, vd= vas deferens). Scale= 4 mm. 

Each vas deferens has an anterior region that is smaller in diameter than the posterior region, and both ducts flow into the anterior region of the ejaculatory duct. The ejaculatory duct is a very elongated organ, with a thick muscular wall that opens to the inner sac, inside the aedeagus (Fig. 1).

There are two accessory glands, each with the anterior glandular region and a posterior glandular duct greater in diameter than the previous one. The glandular region is filamentous, small in diameter, which rolls over on itself and measures approximately 42 mm long. The glandular duct, larger in diameter than the glandular region, measures approximately 34 mm. Both glandular ducts open into the anterior part of the ejaculatory duct, next to the vas deferens (Fig. 1).

The males of all the Phyllophaga species examined have two testes with six testicular follicles and their respective vasa deferens, and two accessory glands open to the ejaculatory duct, which continue with the inner sac inside the aedeagus. Only in P. rugipennis (Fig. 6), M. nigripes (Fig. 11) and I. neglectus (Fig. 12) is the ejaculatory duct shorter, and it opens to an ejaculatory bulb with thick muscular walls.

Testes. In all species of Melolonthinae there are six follicles per testis (Fig. 1-12). In Phyllophaga, the six testicular follicles are free, lobed, and dorsoventrally flattened. In I. neglectus they are free, flattened, and lobed as in the species of Phyllophaga, while in M. nigripes (Fig. 11) the testicular follicles are spherical and grouped within an outer membrane. The vas efferens are long and thin, and the vas deferens is long, with thicker walls, as in all species. Likewise, the anterior part of the vas deferens is smaller in diameter than the posterior part.

Accessory glands. The two accessory glands in all species have an anterior region that is glandular, filamentous, long, and small in diameter, but their length varies among species (Table 1). The longest glands, more than 300 mm long, were found in Ph. tenuipilis (Fig. 9). Glands of 100 to 164 mm in length were found in Ph. obsoleta (Fig. 2), Ph. ravida (Fig. 5), Ph. rugipennis (Fig. 6), and Ph. setifera (Fig. 7), and glands 41 to 86 mm long were found in Ph. testaceipennis (Fig. 1), Ph. opaca (Fig. 3), Ph. pruinosa (Fig. 4), Ph. subrugosa (Fig. 8) and Ch. latipes (Fig. 10). The glandular duct varies in size between nine and 34 mm, depending on the species (Table 1). The smallest accessory glands were found in M. nigripes (Fig. 11). Only in this species was a widening observed in the anterior part of the glandular duct, as a glandular reservoir, but it does not occur in any other of the species studied in Melolonthinae.

Table 1 General characteristics of the male reproductive system of 12 species of Melolonthinae, 6 species of Dynastinae, and 3 species of Rutelinae (n = number, * = presence, - = absence). 

Subfamily species Follicles per testis (n) Accessory gland length (mm) Glandula duct length (mm) Ejaculatory duct Ejaculatory bulb
MELOLONTHINAE
Phyllophaga testaceipennis 6 41.9 34.1 * -
Phyllophaga obsoleta 6 116 9 * -
Phyllophaga opaca 6 86.6 13.9 * -
Phyllophaga pruinosa 6 77 12 * -
Phyllophaga ravida 6 117.6 14.9 * -
Phyllophaga rugipennis 6 103.1 31.5 * *
Phyllophaga setifera 6 164 30.2 * -
Phyllophaga subrugosa 6 73 25.3 * -
Phyllophaga tenuipilis 6 312 10 * -
Chlaenobia latipes 6 63 7.5 * -
Macrodactylus nigripes 6 21.2 4.5 * *
Isonychus neglectus 6 37.3 31.3 * *
DYNASTINAE
Cyclocephala jalapensis 6 44.1 9.8 * *
Cyclocephala picta 6 270. 1 20.5 * *
Cyclocephala sexpunctata 6 178. 2 14 * *
Cyclocephala mafaffa 6 348.6 33.2 * *
Cyclocephala lunulata 6 219 24.3 * *
Cyclocephala weidneri 6 298.7 8.6 * *
RUTELINAE
Paranomala marginicollis 6 35.7 15.5 * *
Paranomala semicincta 6 17. 9 29.9 * *
Paranomala cupricollis 6 144.1 57.5 * *

Ejaculatory duct. This duct is very elongated and occurs in all species of Phyllophaga, though in some species it is slightly thicker towards the back (Table 1), as in Ph. testaceipennis (Fig. 1), Ph. pruinosa (Fig. 4) and Ph. rugipennis (Fig. 6).

Ejaculatory bulb. Only Ph. rugipennis (Fig. 6), M. nigripes (Fig. 11), and I. neglectus (Fig. 12) have an ejaculatory bulb (Table 1). This organ was not seen in all the species of Phyllophaga examined, though in Ph. pruinosa (Fig. 4) and Ph. setifera (Fig. 7) the muscular walls of the ejaculatory duct are thickened and are wider than long, which would represent an incipient ejaculatory bulb.

Dynastinae (Fig. 13-18). The male reproductive system in C. jalapensis (Fig. 13) exemplifies the system seen in all the species examined of this subfamily. It consists of two testicles, each with six dorsoventrally flattened free testicular follicles (Table 1), two vas deferens, two accessory glands with their respective glandular duct, and an ejaculatory bulb that opens into the aedeagus.

Figures 13-18 Male reproductive system of six species of Dynastinae species. 13. Cyclocephala jalapensis 14. C. picta Burmeister 15. C. sexpunctata 16. C. mafaffa 17. C. lunulata 18. C. weidneri. Only in C. jalapensis is the complete reproductive system shown, in the other figures only half is shown. (ae= aedeagus, ag= accessory glands, eb= ejaculatory bulb, ed= ejaculatory duct, gd= glandular duct, gr=glandular reservoir, te= testis, vd= vas deferens). Scale= 4 mm. 

Testes. The six species studied have two testicles, each with six flattened and lobed testicular follicles, and the vas efferens are long. The vas deferens are small in diameter in their anterior region and much larger diameter, with thick walls in the posterior region (Fig. 13-18).

Accessory glands. The longest-almost 349 mm long-were found in C. mafaffa (Fig. 16), and the smallest (44 mm) in C. jalapensis (Fig. 13) (Table 1). In all species, these glands are small in diameter. The glandular duct is long, with thick walls.

Ejaculatory duct. This duct is present in all six species (Table 1), although it is very small in C. jalapensis (Fig. 13), C. sexpunctata (Fig. 15), and C. weidneri (Fig. 18). In the other three species, it is elongated (Fig. 14, 16, 17).

Ejaculatory bulb. In the six species studied, there is a well-developed ejaculatory bulb (Table 1), with thick muscular walls (Fig. 13-18).

Rutelinae (Fig. 19-21). The male reproductive system of Paranomala marginicollis (Fig. 19) is typical of all the Rutelinae species examined. It consists of two testicles, each with six testicular follicles (Table 1), with their respective vas efferens, and a vas deferens. There are two very long accessory glands, with their respective glandular duct, the ejaculatory duct, and the ejaculatory bulb. The organs of the reproductive system of these three species have the same distribution plane.

Figures 19-21 Male reproductive system of three species of Rutelinae. 19. Paranomala marginicollis 20. Paranomala cupricollis 21. Paranomala semicincta. Only in P. marginicollis is the complete reproductive system shown, in the other figures only half is shown. (ae= aedeagus, ag= accessory glands, eb= ejaculatory bulb, ed= ejaculatory duct, gd= glandular duct, gr=glandular reservoir, te= testis, vd= vas deferens). Scale= 4 mm. 

Testes. The three species studied have two testicles, each with six-lobed and dorsoventrally flattened testicular follicles. The vas deferens are large in diameter.

Accessory glands. The accessory glands are 144 mm long in P. cupricollis (Fig. 20), but only 17.9 mm in P. semicincta (Fig. 21) (Table 1).

Ejaculatory duct. The ejaculatory duct is short and is present in all species.

Ejaculatory bulb. In the three species studied, there is a well-developed ejaculatory bulb.

Comparative aspects between the males of Melolonthinae, Dynastinae and Rutelinae.

The species examined in this study were similar in terms of the general morphology of their internal genitalia, however, some differences were found.

Testes. In all the species studied there are two testicles with six lobes and flattened testicular follicles and without an outer membrane to contain them (Table 2), except in M. nigripes (Melolonthinae) in which they are spherical and have a membrane that contains them (Fig. 11). The vas deferens is similar in all species and has no seminal vesicle.

Table 2 Species of Scarabaeoidea with two testes and six testicular follicles. 

Species References
MELOLONTHINAE
Anoxia villosa (Fabricius) Bordas, 1900
Amphimallon majale (Razoumowsky) Menees, 1963
Costelytra zealandica (White) Fenemore, 1971, Stringer, 1990
Chlaenobia latipes Bates Martínez et al., present paper
Hymenoplia strigosa (Illiger) Bordas, 1900
Isonychus neglectus (Moser) Martínez et al., present paper
Macrodactylus nigripes Bates Martínez et al., present paper
Melolontha melolontha (Linnaeus) Dufour, 1825; Straus-Dürckheim, 1828; Bordas, 1900
Phyllophaga anxia LeConte Berberet & Helms, 1972
Phyllophaga obsoleta (Blanchard) Martínez et al., present paper
Phyllophaga opaca (Moser) Martínez et al., present paper
Phyllophaga pruinosa (Blanchard) Martínez et al., present paper
Phyllophaga ravida (Blanchard) Martínez et al., present paper
Phyllophaga rugipennis (Schauffus) Martínez et al., present paper
Phyllophaga setifera (Burmeister) Martínez et al., present paper
Phyllophaga subrugosa (Moser) Martínez et al., present paper
Phyllophaga tenuipilis (Bates) Martínez et al., present paper
Phyllophaga testaceipennis (Blanchard) Martínez et al., present paper
DYNASTINAE
Cyclocephala jalapensis Casey Martínez et al., present paper
Cyclocephala lunulata Burmeister Martínez et al., present paper
Cyclocephala mafaffa Burmeister Martínez et al., present paper
Cyclocephala picta Burmeister Martínez et al., present paper
Cyclocephala sexpunctata Castelnau Martínez et al., present paper
Cyclocephala weidneri Endrödi Martínez et al., present paper
Oryctes nasicornis (Linnaeus) Straus-Dürckheim, 1828
Oryctes rhinoceros (Linnaeus) Mathur et al., 1960; Jacob 1989
RUTELINAE
Anisoplia agricola (Poda) Bordas, 1900
Anomala ausonia Erichson Lupo, 1947
Paranomala cupricollis (Chevrolat) Martínez et al., present paper
Paranomala marginicollis (Bates) Martínez et al., present paper
Paranomala semicincta (Bates) Martínez et al., present paper
Phyllopertha horticola (Linnaeus) Rittershaus, 1927
Popillia japonica Newman Williams, 1945; Anderson, 1950
HOPLIINI
Hoplia argentea (Poda) Bordas, 1990
Hoplia squamifera Burmeister Carrillo-Ruiz et al., 2008
Hoplia subcostata Bates Carrillo-Ruiz et al., 2008
TROGIDAE
Omorgus omacanthus (Harold) Sharp & Muir, 1912
Trox scaber (Linnaeus) Sharp & Muir, 1912
GEOTRUPINAE
Anoplotrupes stercorosus (Scriba) Pluot & Martínez, 1998; Martínez & Cruz, 1999
Bolbocerosoma farctum (Fabricius) Williams, 1945
Bolbelasmus gallicus (Mulsant) Bordas, 1900
Ceratotrupes bolivari Halfft. & Mtz. Pluot & Martínez, 1998; Martínez & Cruz, 1999
Geotrupes mutator (Marsham) Bordas, 1900
Geotrupes stercorarius (Linnaeus) Bordas, 1900
Halffterius rufoclavatus (Jekel) López-G., 1987; Martínez & Cruz, 1999; Trotta et al., 2007
Megatrupes cavicollis Bates Pluot & Martínez, 1998; Martínez & Cruz, 1999
Onthotrupes herbeus (Jekel) Pluot & Martínez, 1998; Martínez & Cruz, 1999
Onthotrupes nebularum (Howden) Pluot & Martínez, 1998; Martínez & Cruz, 1999
Onthotrupes sobrinus (Jekel) Pluot & Martínez, 1998; Martínez & Cruz, 1999
Trypocopris vernalis (Linnaeus) Pluot & Martínez, 1998; Martínez & Cruz, 1999
Typhaeus typhoeus (Linnaeus) Bordas, 1900
SCARABAEINAE
Ateuchetus semipunctatus (Fabricius) Dajoz, 1972
Ateuchus illaesus Harold Martínez & Cruz, 1999
Canthidium moestum Harold Martínez & Cruz, 1999
Canthidium puncticolle Harold Pluot & Martínez, 1998
Canthon cyanellus LeConte Mtz. & Benítez, 1988; Pluot & Mtz., 1998; Mtz. & Cruz, 1999
Canthon femoralis Chevrolat Martínez & Cruz, 1999
Canthon humectus (Say) Pluot & Martínez, 1998; Martínez & Cruz, 1999
Canthon indigaceus LeConte Martínez, 1991; Pluot & Martínez, 1998
Canthon pilularius (Linnaeus) Cooper, 1938
Canthon subhyalinus Harold Martínez & Cruz, 1999
Canthon viridis Palisot de Beauvois Martínez & Cruz, 1999
Copris armatus Harold Pluot & Martínez, 1998; Martínez & Cruz, 1999
Copris incertus Say Cruz & Huerta, 1998; Pluot & Mtz., 1998; Martínez & Cruz, 1999
Copris laeviceps Harold Pluot & Martínez, 1998; Martínez & Cruz, 1999
Copris lugubris Boheman Pluot & Martínez, 1998; Martínez & Cruz, 1999
Copris sierrensis Matthews Pluot & Martínez, 1998; Martínez & Cruz, 1999
Coprophanaeus corythus (Harold) Pluot & Martínez, 1998; Martínez & Cruz, 1999
Coprophanaeus lancifer (Linnaeus) Edmonds, 1974
Coprophanaeus pluto (Harold) Pluot & Martínez, 1998; Martínez & Cruz, 1999
Deltochilum gibbosum (Fabricius) Martínez & Cruz, 1999
Deltochilum lobipes Bates Pluot & Martínez, 1998; Martínez & Cruz, 1999
Deltochilum pseudoparile Paulian Pluot & Martínez, 1998; Martínez & Cruz, 1999
Dichotomius carolinus (Linnaeus) Williams, 1945, Pluot & Martínez, 1998
Dichotomius centralis (Harold) Pluot & Martínez, 1998; Martínez & Cruz, 1999
Dichotomius satanas (Harold) Pluot & Martínez, 1998; Martínez & Cruz, 1999
Euoniticellus intermedius (Reiche) Pluot & Martínez, 1998; Martínez & Cruz, 1999
Eurysternus caribaeus (Herbst) Pluot & Martínez, 1998; Martínez & Cruz, 1999
Eurysternus mexicanus Harold Pluot & Martínez, 1998; Martínez & Cruz, 1999
Gromphas inermis Harold Martínez & Cruz, 1999
Liatongus rhinocerulus (Bates) Pluot & Martínez, 1998; Martínez & Cruz, 1999
Ontherus mexicanus Harold Pluot & Martínez, 1998; Martínez & Cruz, 1999
Onthophagus aureofuscus Bates Martínez & Cruz, 1999
Onthophagus batesi Howden & Cart. Pluot & Martínez, 1998; Martínez & Cruz, 1999
Onthophagus chevrolati Harold Pluot & Martínez, 1998; Martínez & Cruz, 1999
Onthophagus cyanellus Bates Pluot & Martínez, 1998; Martínez & Cruz, 1999
Onthophagus hippopotamus Harold Pluot & Martínez, 1998; Martínez & Cruz, 1999
Onthophagus incensus Say Pluot & Martínez, 1998; Martínez & Cruz, 1999
Onthophagus rhinolophus Harold Pluot & Martínez, 1998; Martínez & Cruz, 1999
Onthophagus rostratus Harold Pluot & Martínez, 1998
Onthophagus vacca Linnaeus Pluot & Martínez, 1998
Phanaeus amethystinus Harold Martínez & Cruz, 1999
Phanaeus demon Castelnau Martínez & Cruz, 1999
Phanaeus endymion Harold Pluot & Martínez, 1998; Martínez & Cruz, 1999
Phanaeus scutifer Bates Pluot & Martínez, 1998
Phanaeus tridens Castelnau Pluot & Martínez, 1998; Martínez & Cruz, 1999
Sulcophanaeus menelas (Castelnau) Martínez & Cruz, 1999

Accessory glands (Table 1). These glands differ in length depending on the species of each subfamily. In Melolonthinae, they range from 21.2 mm as in M. nigripes (Fig. 11) to 117.6 mm as in Ph. ravida (Fig. 5), except in Ph. tenuipilis (Fig. 9) in which they measured 312 mm. In Dynastinae, these glands were very long in five of the six species examined: 178.2 mm in C. sexpunctata (Fig. 15), 219 mm in C. lunulata (Fig. 17), 270 mm in C. picta (Fig. 14), 298.7 mm in C. weidneri (Fig. 18) and 348.6 in C. mafaffa (Fig. 16); whereas in C. jalapensis (Fig. 13) they only measured 44.1 mm. In the three species of Rutelinae, the length of these glands also varied among species, in P. semicincta (Fig. 21) they measured 17.9 mm, in P. marginicollis (Fig. 19) 35.7 mm and in P. cupricollis (Fig. 20) 144.1 mm. Only in M. nigripes (Fig. 11) is there a glandular reservoir on each side, which was not observed in any other species.

Ejaculatory duct (Table1). This duct is present in all species but varies in length. This duct is long in Melolonthinae species (Fig. 1-5, 7-10), except in Ph. rugipennis (Fig. 6), M. nigripes (Fig. 11) and I. neglectus (Fig. 12), in which the back of the ejaculatory duct thickens forming an ejaculatory bulb. Ejaculatory bulb (Table 1). This organ occurs in three species of Melolonthinae: Ph. rugipennis (Fig. 6), M. nigripes (Fig. 11) and I. neglectus (Fig. 12), and in all Dynastinae (Fig. 13-18) and Rutelinae (Fig. 19-21) species.

DISCUSSION

Testes and vasa deferens. In all species studied there are six testicular follicles as occurs in the species of other Scarabaeoidea subfamilies (Table 2). However, in species of Passalidae there are two testicular follicles (Krause, 1946; Cruz & Castillo, 2008; Salazar et al., 2016), whereas species of Aphodiinae have six to seven testicular follicles, while some species of Eupariini have two testicular follicles (Martínez et al., 2001) and Lucanidae have twelve (Reyes-Castillo et al., 2004).

The vas deferens are similar in all the species of the three subfamilies studied and in none of them was a seminal vesicle observed. Nevertheless, the presence of a seminal vesicle has been observed in other Melolonthinae species: Prodontria lewisii Broun, 1904 and Costelytra zealandica (White, 1846) (Ferreira & McKinlay, 2001; Stringer, 1990). But, in two species of Hoplia (Carrillo-Ruiz et al., 2008) in reality the seminal vesicle is only a dilation of the final part of the vas deferens. In one species of Dynastinae, Oryctes rhinoceros (Linnaeus, 1758) (Jacob, 1989; Mathur et al., 1960), the seminal vesicle appears as an elongated dilation in the middle of the vas deferens. And in one species of Rutelinae, Plusiotis costata (Blanchard, 1851), it appears as two independent hemispherical dilations between the anterior and posterior vas deferens (Morón, 2010).

Accessory gland. These glands are very long in Melolonthinae, Dynastinae, and Rutelinae. In fact, these glands are much longer than those of the other scarab species that have been studied (Berberet & Helms, 1972; Jacob, 1989; Diefenbach et al., 1998; Stringer, 1990; Carrillo-Ruiz et al., 2008; Morón 2010). The glandular reservoir, which is located between the gland and the glandular duct, was only observed in M. nigripes (Fig. 11). This organ was also observed in M. mexicanus and O. rhinoceros (Mathur et al., 1960; Benítez-Herrera et al., 2015). Some authors call the final part of the glandular duct the “glandular reservoir”, perhaps because that region is very wide, but it is not a glandular reservoir.

Ejaculatory duct. This duct is straight and long in the Melolonthinae species studied (Fig. 1-5, 7-10) except in Ph. rugipennis, M. nigripes and I. neglectus, in which the back of the ejaculatory duct thickens to form an ejaculatory bulb (Fig. 6, 11, 12). A long duct is also reported for other Melolonthinae such as C. zealandica and M. mexicanus (Stringer, 1990; Benítez-Herrera et al., 2015). It has also been described as a short duct in P. anxia and P. sanctipauli (Berberet & Helms, 1972; Diefenbach et al., 1998). In Dynastinae and Rutelinae, the ejaculatory duct is short before entering the ejaculatory bulb in all the species examined, as observed in O. rhinoceros and Ch. costata (Mathur et al., 1960; Jacob, 1989; Morón, 2010).

Ejaculatory bulb. This organ occurs in three species of Melolonthinae, Ph. rugipennis, M. nigripes, and I. neglectus, and in all species of Dynastinae and Rutelinae (Table 1). It has also been observed in Ph. anxia (Berberet & Helms, 1972), though these authors refer to it as the "erection fluid pump". It is also present in Ph. sanctipauli (Diefenbach et al., 1998) and C. zealandica (Stringer 1990), for which the latter author calls it the “muscular sheath of ductus ejaculatorius”, and in M. mexicanus (Benítez-Herrera et al., 2015). In the genus Hoplia, the ejaculatory bulb is found in H. squamifera and H. subcostata (Carrillo-Ruiz et al., 2008), and these authors referred to it as the “ejaculatory duct”. In Dynastinae there is an ejaculatory bulb in O. rhinoceros (Mathur et al., 1960; Jacob, 1989), which the latter author refers to as the “spermatophore sac”. In Rutelinae it occurs in C. costata (Morón, 2010).

In species of Aphodiinae and Scarabaeinae, it is known that the ejaculatory bulb, a complex muscular structure that contains the ejaculatory duct of ectodermal origin, is well developed. In Aphodius pseudolividus (Aphodiinae), the ejaculatory bulb is formed by a thick (50 µm) muscular wall, inside of which is the ejaculatory duct and a part of the internal sac. In Canthon indigaceus (Scarabaeinae) this structure is more complicated, with a 100 µm thick muscular wall and, in addition to the ejaculatory duct, there is a third gland that is ectodermal in origin (an ectadenia). Its structure indicates that it has a pumping function; the muscular contractions probably ensure the emission of the secretions of the accessory glands and the seminal fluid with the spermatozoa, which participate in the formation of the spermatophore (Pluot-Sigwalt & Martínez, 1998). Perhaps the complexity of the ejaculatory bulb is related to the shape of the spermatophore. The spermatophore of several Scarabaeinae species is more elaborate than that of Aphodiinae species (Cruz & Martínez, 1992; Martínez, 2003) and in other Scarabaeoidea species its shape is very simple, including Melolontha melolontha (Landa, 1960), Costelytra zealandica (Striger, 1988) and Phyllopertha horticola (Rittershaus, 1927). In the species studied, the spermatophore is still unknown.

Acknowledgments

The present study is dedicated to Miguel Ángel Morón, a brilliant world-renowned entomologist, who dedicated his life to the study of Melolonthinae in Latin America and passed in 2017. We thank the Instituto de Ecología, A. C. (Xalapa, Veracruz, Mexico) for support, and Ricardo Madrigal Ch. for help with the laboratory work. Ana Kory Martínez and Bulmaro Cano prepared the initial illustrations and Bianca Delfosse revised the English. We are grateful to three anonymous reviewers for their valuable contributions to improving the manuscript.

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Responsible editor: Magdalena Cruz-Rosales

Cite: Martínez, M. I., Rivera-Gasperín, S. L., Carrillo-Ruiz, H., Morón, M. A. (2021) Comparative aspects of the internal reproductive system of males in species of Melolonthinae, Dynastinae, and Rutelinae (Coleoptera: Scarabaeoidea) from Mexico. Acta Zoológica Mexicana (nueva serie), 37, 1-17. 10.21829/azm.2021.3712419. elocation-id: e3712419

Received: May 19, 2021; Accepted: August 26, 2021

*Corresponding author: Imelda Martínez M. imelda.martinez@inecol.mx

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