Biology and management of the masked chafer Cyclocephala distincta Burmeister (Melolonthidae, Dynastinae, Cyclocephalini)

Abstract

Adults of Cyclocephala distincta are flower visitors of Neotropical palms (Arecaceae) and commonly found in the Atlantic Forest of Pernambuco, Brazil. Males and females were collected in the wild and subjected to captive rearing and breeding. The egg hatching rate, the life cycle, longevity of immatures and adults, and oviposition parameters in captivity were analyzed. The average duration of the life cycle of C. distincta was 108.2 days (n = 45). The egg stage lasted on average 10.9 days, and the egg-hatching rate was 73.9%. The immature stage lasted on average 93.4 days. The larvae stage exhibited negative phototaxis, and the size of their head capsules increased at a constant rate of 1.6 between instars, following Dyar's rule. The average duration of the first instar was 24.8 days (n = 88), whereas the second and third instars lasted for 17.2 (n = 76) and 40.4 (n = 74) days respectively, and survival rates were 21.6%, 86.4% and 97.4%. The pre-pupal stage was recorded, and pupal chambers were built before pupation. The average number of eggs laid per female was 15.5, the total reproductive period lasted for 3.3 days, and the total fertility was 81.2%. Adults that emerged in captivity exhibited an average longevity of 18.9 days. Adult C. distincta exhibited thanatosis behavior upon manipulation, a strategy observed for the first time in Cyclocephala.

Breeding; Life cycle; Rearing; Thanatosis

Introduction

One group of insects which stands out for including highly specialized pollinators are the scarab beetles of the tribe Cyclocephalini, often associated with attractive floral scent volatiles produced by their host plants during episodes of floral thermogenesis (Bernhardt, 2000; Gottsberger, 1990, 1999; Gottsberger and Amaral, 1984; Gottsberger and Silberbauer-Gottsberger, 1991). Cyclocephala Dejean contributes with over 85% of the richness of cyclocephaline scarabs, with about 500 described species (Ratcliffe et al., 2013). Little is known about the biology of Cyclocephala, but it is generally observed that the adults of many species exhibit crepuscular/nocturnal habits (Ratcliffe, 2008; Riehs, 2006) and feed on pollen, flower parts and nutritious exudates produced by the flowers they visit (Gibernau et al., 1999; Gottsberger, 1986).

Females of Cyclocephala lay their eggs directly on soil (Mondino et al., 1997; Santos and Ávila, 2007). The larvae dwell underground, where they feed on grass roots, decaying organic matter or on the petioles of plants (Grebennikov and Scholtz, 2004; Ponchel, 2006; Ratcliffe, 2003; Ratcliffe and Cave, 2006; Stechauner-Rohringer and Pardo-Locarno, 2010). Depending on the feeding substrate, the larvae can either be treated as contributors to the environmental balance (Gassen, 2000) or destructive agricultural pests (Potter et al., 1996; Ritcher, 1966). The biological cycle of Cyclocephala is considered univoltine (it was described as bivoltine only for C. lunulata Burmeister, 1847), however, it has only been studied in about 1% of the currently described species (Cherry, 1985; Gavotto, 1964; Nogueira et al., 2013; Rodrigues et al., 2010; Santos and Ávila, 2007; Souza et al., 2014; Stechauner-Rohringer and Pardo-Locarno, 2010).

Cyclocephala distincta Burmeister, 1847 is native to the Guianas, Colombia and Brazil. Adults of the species are known flower visitors of palms, and even assumed as likely pollinators of some species (Arecaceae) (Endrödi, 1985; Voeks, 2002). However, interactions of the larvae with plants are currently unknown. Larvae of several other congenerics have been historically documented as pests (Bran et al., 2006; Potter et al., 1996). Nonetheless, most of these species have only been poorly studied regarding their biology, including C. distincta, thus hindering the development of strategies for the conservation of native pollinators and efficient pest management. This work aims to evaluate the biological aspects of Cyclocephala distincta through the analysis of egg-hatching rates, the life cycle and oviposition parameters.

Material and methods

Adult C. distincta (n = 227) were collected in the wild at the Campo de Instrução Marechal Newton Cavalcante (07°50' S; 35°06' W, Abreu e Lima, Pernambuco, Brazil). The CIMNC fragment is considered one of the largest continuous patches of the Atlantic Forest north of the São Francisco River, with lowland dense rainforest (IBGE, 1992). Sampling was carried for three months (December 2010, January and February 2011), between 6:00 p.m. and 5:00 a.m., using light traps. The trap consisted of a vertical white cloth illuminated by a black light 250W, during the new, growing or waning moon stages, when most nocturnal insects exhibit a lower discernment between natural and artificial light sources (Almeida et al., 2012; Nowinszky, 2004). The breeding in captivity was reared under natural environmental conditions of temperature (29.3 ± 0.7 °C) and relative humidity (56 ± 1.9%), and a fixed photoperiod of 12:12h.

Egg-hatching rate and life cycle. A total of 127 adults were kept in plastic terraria (4 dm³⁾ filled with circa 3 dm³ of potting soil (Gnúmus Ltda). On average, 25 individuals of C. distincta (2 ♀: 1 ♂) were allocated per terrarium. A diet of fresh sliced apples and plantains was offered to the beetles (roughly 3.0 g per individual) and replenished every three days (Lai and Shin-ping, 2008; McMonigle, 2006; Souza et al., 2014). Egg-hatching rate, size, viability, coloration, duration, longevity, and behavior of each stage of life cycle were observed. The total duration of life cycle and longevity of adults emerged in captivity were compared between the sexes through Student's t test.

The immature stages were maintained as following:

Egg: On a daily basis, freshly oviposited eggs were removed from the terraria and placed in smaller plastic containers (250 cm³⁾ also filled with c. 167cm³ of potting soil (Gnúmus Ltda).

Larvae: Immediately after hatching, the larvae were transferred to individual plastic containers (250 cm³⁾ also filled with c. 167 cm³ of potting soil (Gnúmus Ltda). To feed the larvae, we prepared an even mix of fresh humus (Gnúmus LTDA) and finely pulverized dead wood and crushed leaf-litter (c. 50 g) that was collected at the site where the adults were captured. This feeding substrate was replenished every three days.

Pre-pupa and pupa: The larvae that reached the pre-pupal stage, and then pupated, were kept in the same containers. Food supply was interrupted.

Females of C. distincta captured in the wild (n = 100) were individually placed in plastic containers (250 cm³⁾ filled with 167 cm³ of potting soil (Gnúmus LTDA) and fed with a diet of sliced apples and plantains (roughly 3.0 g per individual), replenished every three days (Lai and Shin-ping, 2008; McMonigle, 2006; Souza et al., 2014). To estimate the oviposition parameters, we recorded the pre-oviposition period (time interval between the day of capture to the first posture); number of postures per female; number of eggs per posture; inter-posture period; total reproductive period (interval between the first and last posture in captivity), and overall fertility (ratio of the total number of larvae and total number of eggs).

Results and discussion

During sunlight hours, adult beetles kept in the terraria buried themselves in the substrate and displayed no other activities that could be visualized. Copulation and feeding occurred during nighttime (between 6:00 p.m. and 8:00 p.m.), but independently of each other. In other species of the genus, mating activities were not restricted to any period of the day (Rodrigues et al. [2010]for C. verticalis Burmeister, 1847; and Souza et al. [2014] for C. celata Dechambre, 1980). Adult C. distincta exhibited negative phototaxis, and when handled exhibited thanatosis (Fig. 1). This behavior was characterized by the retraction of all legs and lack of movement from the antennae and maxillary palps. This is the first record of thanatosis for the genus.

Figure 1.
Male Cyclocephala distincta exhibiting thanatosis behavior. Adult mean size: 10 mm.

Larvae hatching rate and life cycle

Egg

Each egg was accommodated inside an individual cell built by the female out of the soil substrate of the terraria. About 80% of these egg cells were entirely closed, while the remainder exhibited a small opening (approx. 3 mm diameter). The construction of egg cells had been previously described for C. verticalis, C. signaticollis Burmeister, 1847, C. melanocephala (Fabricius, 1755), C. tucumanaBrethes, 1904, C. paraguayensis Arrow, 1913 and C. celata (Albuquerque et al., 2014; Morelli, 1991; Nogueira et al., 2013; Rodrigues et al., 2010; Souza et al., 2014) and it is assumed to be a strategy of parental care, since it offers extra protection to the fragile, recently oviposited eggs (Triplehorn and Jonnson, 2011). According to Potter and Gordon (1984), the shell of freshly oviposited eggs of C. luridaBland, 1863 is thin and highly susceptible to desiccation. The same authors also observed that larvae of this species that hatched from eggs subjected to water stress were significantly smaller in size and were sometimes unable to disengage from the chorion membrane.

Freshly oviposited eggs of C. distincta were in average 1.2 mm long and 1.0 mm wide (n = 30), elliptically shaped, and exhibited a whitish color. During embryonic development, the eggs gradually increased in size and assumed a spherical shape, as previously observed for C. signaticollis, C. parallela Casey, 1915, C. paraguayensis and C. celata (Albuquerque et al., 2014; Cherry, 1985; Gavotto, 1964; Souza et al., 2014). The increase in egg size is due to the absorption of water during growth and is made possible by the serosal layer of the egg membrane (Hinton, 1981). The egg stage lasted 10.9 ± 0.2 days (n = 408). Egg-hatching rate was 73.9% (Table 1).

Table 1.
Duration (mean ± DP), interval variation, viability (%), and number of specimens (N) of development stages of Cyclocephala distincta in captivity.

Stage	Duration (days)	Interval variation	Viability (%)	N
Egg	10.9 ± 0.2	9-14	73.9	408
1st instar	24.8 ± 5.6	17-42	21.6	88
2nd instar	17.2 ± 1.9	9-26	86.4	76
3rd instar	40.4 ± 2.3	28-55	97.4	74
Pre-pupa	3.9 ± 1.5	2-10	90	67
Pupa	11 ± 0.6	7-15	67.2	45
Adult ♀	20.2 ± 8.4	4-36	–	24
Adult ♂	17.4 ± 8.2	4-29	–	21
Egg to adult	108.2 ± 11	90-137	8.2	45

Larvae

Both the head and body of newly hatched larvae exhibited a whitish-transparent coloration. One day after hatching, the head assumed an orange coloration, and the body became transparent. The larvae exhibited negative phototaxis and defecated when handled (Fig. 2A). Although no distinguishable odor was detected in the feces of C. distincta, the release of fecal material is a widely recognized defense mechanism developed by various animal taxa (Alpert and Ritcher, 1975). The released odor may repel possible predators and increase the chances of survival of the prey (Alpert and Ritcher, 1975). The behavior of defecation when handled was similar to that of C. verticalis (Coutinho et al., 2011).

Figure 2.
Larval stage of Cyclocephala distincta bred in captivity. A, Larva of the 2nd instar defecating (mean size: 1.3 mm); B, Cephalic capsule of the 1st, 2nd and 3rd instars, respectively; C, Transition between the 3rd instar (below) and pre-pupa (above).

Three larval instars were recorded in C. distincta, easily distinguishable from one another by abrupt changes of the maximum width of the head capsule (Fig. 2B), which increased at a constant rate of 1.6 (1.0-1.6-2.6 mm), following the Dyar's rule (1890). The same rate of increase was found in C. fosteriEndrödi, 1963 and C. paraguayensis (Albuquerque et al., 2014; Santos and Ávila, 2007). The intervals between successive larval instars (1^st-2^nd, 2^nd-3^rd, 3^rd-pre-pupal) were respectively 24.8 ± 5.6 (n = 88), 17.2 ± 1.9 (n = 76) and 40.4 ± 2.3 days (n = 74), and survival rates were 21.6%, 86.4% and 97.4%.

As a general rule, the longest interval of the life cycle of holometabolous insects is spent during the larval stage, a period during which they must secure nutritional resources that may be allocated to support growth and/or reproduction in the adult stage (Chapman, 1998). During the larval stage of C. distincta, the 3^rd instar was the longest, a feature shared with other congenerics (Albuquerque et al., 2014; Cherry, 1985; Mondino et al., 1997; Rodrigues et al., 2010; Santos and Ávila, 2007; Souza et al., 2014) and even with other pest species of scarabs (Ávila and Santos, 2009). Because it is the longest, individuals at the 3^rdinstar exhibit a more pronounced food intake than at the previous instars, and consequently this stage is considered the most damaging to crops (Ávila and Santos, 2009; Oliveira, 2007; Pereira and Salvadori, 2006).

Pre-pupa and pupa

At the end of the 3^rd instar, the larvae of C. distinctaconstructed a pupal cell with soil from the rearing substrate. They remained inside it without food, with consequent weight loss (Mondino et al., 1997), until their emergence as imagoes. The silk and other secretions that cement the particles used to build the pupal cells are generally produced by the Malpighian tubules, peritrophic membrane or glands that open on the last abdominal tergite and are connected to the anus (Costa et al., 1988). During 3.9 ± 1.5 days (n = 67) prior to pupation, individuals of C. distincta remained in the pre-pupal stage, characterized by a milky-white colored tegument, which is thinner and transparent in the abdominal segments VIII, XI and X (Fig. 2C). When handled, the pre-pupae reacted by stretching their bodies, which were previously curved in a characteristic "C" shape.

Ninety percent of the pre-pupae reached the pupal stage. The pupae possessed a yellowish tegument and presented circular mobility of the terminal portion of the abdomen. The stage lasted for 11 ± 0.6 days and was similar only to what had been previously observed for C. paraguayensis (Albuquerque et al., 2014; Cherry, 1985; Mondino et al., 1997; Nogueira et al., 2013; Rodrigues et al., 2010; Santos and Ávila, 2007; Souza et al., 2014). We recorded an emergence rate of 67.2% (n = 45), 21 males and 24 females. We noticed that light-trappings of C. distincta yielded more female than male captures, a fact also observed for other congenerics, such as C. clarae Höhne, 1923, C. paraguayensis, C. suturalis Ohaus, 1911, and C. variolosa Burmeister, 1847 (Riehs, 2006).

According to Fisher (1930), a population will only reach stability when its sex ratio is 1:1. A deviating sex ratio shift is not evolutionarily stable, because gradual increases of individuals belonging to the less abundant sex will occur in future generations. Typically, these deviations are explained by theories involving (1) demographic factors (Otsuka and Koshio, 1999; Yanega, 1996, 1997), (2) local competition for mating and/or inbreeding (Cowan, 1991; Hamilton, 1967), and (3) differential availability of resources in terms of quantity and/or quality (Charnov, 1982; Schwarz, 1988). Nonetheless, specific studies are in order because it is plausible that the putative unbalanced sex ratio observed for C. distincta is merely the result of a higher attractiveness of females to artificial light sources (Kober, 1982).

Adult

The newly emerged adults (Fig. 3A) exhibited pale beige-colored elytra, membranous wings not folded under the elytra, defined stains on the pronotum, and poorly-defined stains on the elytra, as well as limited mobility. One day after emergence (Fig. 3B), the elytra of the beetles assumed a dark beige coloration, hind wings folded under the elytra, stains on the elytra became defined, the insects showed improved mobility, and when handled they presented thanatosis behavior and released a transparent liquid from the anus (Fig. 3C). The discharge of liquids from the anus generally has a defensive function (Chapman, 1998).

Figure 3.
Adult Cyclocephala distincta bred in captivity. A, Newly hatched male; B, Male one day after hatching; C, Liquid-releasing behavior. Adult mean size: 10 mm.

Life cycle

The complete life cycle of C. distincta, from an egg to a new adult, lasted on average 108.2 ± 11 days; 112.3 ± 11.6 [range: 90, 137] for females and 103.9 ± 8.5 [92, 116] for males, with a significant difference of the duration of the cycle between the sexes (p < 0.05; 0.0091). In many insects, males complete the sexual development before their female siblings. This hastier sexual maturation of the males can sometimes be sexually selected (Thornhill and Alcock, 1983). Among species in which the emergence of both sexes is synchronized, the most precocious males will potentially have more chances of finding mates (e.g. Gwynne, 1980), whereas in species with less obvious synchrony, the development may reflect sexually dimorphic patterns of growth and nutritional needs (e.g. Cicero, 1988).

The adults emerged in captivity had an average longevity of 18.9 ± 8.3 days; 20.2 ± 8.4 [4, 36] for females and 17.4 ± 8.2 [4, 29] for males, with no significant difference in longevity between sexes (p > 0.05; 0.1055). Virgin females emerged in captivity did not lay eggs. The C. tucumana and C. melanocephalaadults emerged in captivity had an average longevity of 13.3 and 26.0 days respectively (Nogueira et al., 2013).

The complete life cycle of C. distincta in captivity is the shortest among all known species of Cyclocephala. A rough analysis of the environmental conditions in captivity shows that ambient temperatures throughout the duration of the experiment with C. distincta were higher than those under which other congenerics were reared (Mondino et al., 1997; Rodrigues et al., 2010; Santos and Ávila, 2007; Souza et al., 2014). Because cyclocephaline scarabs are endothermic, environmental temperatures strongly influence their metabolism (Seymor et al., 2009). Thus, under higher temperatures, the life cycles of these insects are completed faster than they would be at lower temperatures (Duarte and Polanía, 2009; Galvão et al., 1999; Triplehorn and Jonnson, 2011).

Our results show that the larvae of C. distincta grow well and healthy when fed an exclusively saprophagous diet. A comparison of the survival rate of C. distincta (egg to adult) observed in the current study with that of C. verticalis, whose larvae were fed with living roots of grasses (Rodrigues et al., 2010), evidenced a difference of only 0.9%. Captivity rearing and breeding of beetles of the genus Cyclocephala are usually performed using living roots of grasses for larval feeding (Miner, 1948; Rodrigues et al., 2010). However, there are records of some species (C. amazona (Linnaeus, 1767), C. lunulata, C. fulgurata Burmeister, 1847, C. stictica Burmeister, 1847, C. paraguayensis and C. celata) that are identified as facultative saprophages, thus capable of undergoing their entire life cycle without feeding on living plant tissue (Albuquerque et al., 2014; Pardo-Locarno et al., 2005; Souza et al., 2014).

Oviposition parameters

Of the 171 females collected in the field, 57% laid eggs, and the pre-oviposition period was in average 3.7 ± 1.6 days [1, 7] long. We recorded one to three postures per female. The number of postures per female and the corresponding average number of eggs laid per female were: one posture (n = 24), 16.7 ± 5.9 eggs; two postures (n = 22), 13.5 ± 6.9 eggs, and three postures (n = 11), 16.4 ± 5.4 eggs. Female C. signaticollis laid in average 17 eggs, and C. tucumana laid 6.5 to 10.8 eggs, but the number of postures per individual was not recorded (Gavotto, 1964; Nogueira et al., 2013). Our results show that the number of eggs laid per female tends to be similar, regardless of the number of postures. Distributing the eggs in more than one posture could be a strategy to minimize the pressure of predation and/or parasitism under natural conditions (Zanuncio et al., 1992).

Females that made two postures laid an average of 8.3 ± 6.6 and 5.3 ± 6.1 eggs in the first and second postures, respectively, and those that laid their eggs in ​​three postures had an average of 7.6 ± 6.9, 6.0 ± 4.4, and 2.8 ± 1.7 eggs in the consecutive events (Fig 4). These results show a tendency of decrease in the number of eggs per posture. This may be a strategy to preserve oocytes until a new copulation occurs, since the females are under conditions of nutritional stress and the males assist them with nutritional contribution during copulation, as has been observed in many insects (Ganho and Marinoni, 2000; Wheller, 1996).

Figure 4.
Average number of eggs laid by female Cyclocephala distincta in the 1st, 2nd and 3rd postures. A, females that made one posture; B, females that made two postures; C, females that made three postures.

Gravid females of C. distincta who made only two postures exhibited a longer interval between them, in average 2.4 ± 0.9 days. On the other hand, females that made three postures did so in an interval of 1.3 ± 0.5 days between the first and second postures, and of 1.7 ± 2.1 days between the second and the third postures. The total reproductive period lasted for 3.3 ± 2.3 days [1, 12], and the total fertility was 81.2% (n = 879).

Acknowledgements

We thank Paschoal Coelho Grossi for the identification of adults of Cyclocephala distincta.

References

• Albuquerque, L.S.C., Souza, T.B., Maia, A.C.D., Iannuzzi, L., 2014. New biological and immature morphological records of the masked chafer, Cyclocephala paraguayensis. J. Insect Sci. 14, 1-11.
• Almeida, L.M., Ribeiro-Costa, C.S., Marinoni, L., 2012. Coleta, Montagem, Preservação e Métodos para Estudo. In: Rafael, J.A., Melo, G.A.R., Carvalho, C.J.B., Casari, S.A., Constantino, R. (eds.). Insetos do Brasil: Diversidade e Taxonomia. Holos Editora, Ribeirão Preto, pp. 175-190.
• Alpert, G.D., Ritcher, P.O., 1975. Notes on the life cycle and myrmecophilous adaptations of Cremastocheilus armatus (Coleoptera: Scarabaeidae). Psyche 82, 283-291.
• Ávila, C.J., Santos, V., 2009. Corós associados ao sistema de plantio direto no estado de Mato Grosso do Sul. Doc. Embrapa Agropec. Oeste. 101, 9-34.
• Bernhardt, P., 2000. Convergent evolution and adaptive radiation of beetle-pollinated angiosperms. Plant Sys. Evol. 222, 293-320.
• Bran, A.M., Londoño, M.E., Pardo, L.C., 2006. Morfología de estados inmaduros de tres especies de Cyclocephala (Coleoptera: Melolonthidae) com uma clave para larvas de tercer estado em Colombia. Rev. Corpoica-Ciencia Tec. Agrop. 7, 58-66.
• Chapman, R.F., 1998. The insects: Structure and function. Cambridge University Press, Cambridge.
• Charnov, E.L., 1982. The theory of sex allocation. Princeton University Press, New Jersey.
• Cherry, R.H., 1985. Seasonal phenology of white grubs (Coleoptera: Scarabaeidae) in Florida sugarcane fields. J. Econ. Entomol. 78, 787-789.
• Cicero, J.M., 1988. Ontophylogenetics of cantheroid larviforms (Coleoptera: Cantheroidea). Coleop. Bull. 42, 105-151.
• Costa, C., Vanin, S.A., Casari-Chen, S.A., 1988. Larvas de Coleoptera do Brasil. Museu de Zoologia da Universidade de São Paulo, São Paulo.
• Coutinho, G.V., Rodrigues, S.R., Cruz, E.C., Abot, A.R., 2011. Bionomic data and larval density of Scarabaeidae (Pleurosticti) in sugarcane in the central region of Mato Grosso do Sul, Brazil. Rev. Bras. Entomol. 55, 389-395.
• Cowan, D.P., 1991. The solitary and presocial Vespidae. In: Ross, K.G., Matthews, R.W. (eds.). The social biology of wasps. Cornell University Press, Ithaca, pp. 33-73.
• Duarte, H.W., Polanía, I.Z., 2009. Efecto de la temperatura sobre el desarrollo de Eriopis connexa connexa (Germar) (Coleoptera: Coccinelidae). Rev. UDCA Act. Div. Cient. 12, 135-145.
• Dyar, H.G., 1890. The number of molts of lepidopterous larvae. Psyche 5, 420-422.
• Endrödi, S., 1985. The Dynastinae of the world. Dr W. Junk Publishers, Dordrecht.
• Fisher, R.A., 1930. The genetical theory of natural selection. Clarendon Press, Oxford.
• Galvão, C., Rocha, D.S., Cunha, V., Presgrave, O.A.F., Jurberg, J., Carcavallo, R., 1999. Influência da temperatura no ciclo de vida de Triatoma melanosoma Martínez, Olmedo & Carcavallo, 1987 (Hemiptera, Reduviidae). Mem. Inst. Oswaldo Cruz. 94, 851-854.
• Ganho, N.G., Marinoni, R.C., 2000. Algumas características da reprodução e ontogênese de Epilachna paenulata (Germar) (Coleoptera, Coccinellidae, Epilachninae). Rev. Bras. Zool. 17, 445-454.
• Gassen, D.N., 2000. Os benefícios de corós em lavouras sob plantio direto. Available at: http://www.cnpt.embrapa.br/biblio/p_co47.htm [accessed 25 Nov 2013].
  » http://www.cnpt.embrapa.br/biblio/p_co47.htm
• Gavotto, A.L.R., 1964. Ciclo biológico de Cyclocephala signaticollis Burm. (Col. Scarabaeidae) y caracteres específicos de su larva. Rev. Invest. Agrop. 1, 151-161.
• Gibernau, M., Barabé, D., Cerdan, P., Dejean, A., 1999. Beetle pollination of Philodendron solimoesense (Araceae) in French Guiana. Int. J. Plant Sci. 160, 1135-1143.
• Gottsberger, G., 1986. Some pollination strategies in Neotropical savannas and forests. Plant Sys. Evol. 152, 29-45.
• Gottsberger, G., 1990. Flowers and beetles in the South American tropics. Botanica Acta. 103, 360-365.
• Gottsberger, G., 1999. Pollination and evolution in neotropical Annonaceae. Plant Spec. Biol. 14, 143-152.
• Gottsberger, G., Amaral Jr., A., 1984. Pollination strategies in Brazilian Philodendron species. Ber. Deut. Bot. Ges. 97, 391-410.
• Gottsberger, G., Silberbauer-Gottsberger, I., 1991. Olfactory and visual attraction of Erioscelis emarginata (Cyclocephalini, Dynastinae) to the inflorescences of Philodendron selloum (Araceae). Biotropica 23, 23-28.
• Grebennikov, V.V., Scholtz, C.H., 2004. The basal phylogeny of Scarabaeoidea (Insecta: Coleoptera) inferred from larval morphology. Invert. Sys. 18, 321-348.
• Gwynne, D.T., 1980. Female defense polygyny in the bumblebee wolf, Philanthus bicinctus (Hymenoptera, Sphecidae). Behav. Ecol. Sociobiol. 7, 213-225.
• Hamilton, W.D., 1967. Extraordinary sex ratios. Science 156, 477-488.
• Hinton, H.E. 1981., The biology of insect eggs. Volume I. Pergamon Press.
• IBGE (Fundação Instituto Brasileiro de Geografia e Estatística). 1992. Atlas Nacional do Brasil. IBGE.
• Kober, E.A.M., 1982. Armadilha luminosa: informações técnicas. Emater, Porto Alegre.
• Lai, J., Shin-ping, K., 2008. For the love of rhinoceros and stag beetles. 2nd ed. Vols. 1, 2. Morning Star Publisher.
• McMonigle, O., 2006. The complete guide to rearing flower and jewel scarabs. Elytra and Antenna Insect Books.
• Miner, F.D., 1948. Rearing technique for white grubs. J. Kansas Entomol. Soc. 21, 58-59.
• Mondino, E.A., López, A.N., Alvarez-Castillo, H.A., Carmona, D.M., 1997. Ciclo de vida de Cyclocephala signaticollis Burmeister, 1847 (Coleoptera: Scarabaeidae: Dynastinae) y su relación con los factores ambientales. Elytron 11, 145-156.
• Morelli, E., 1991. Descripción de la larva y de la pupa de Cyclocephala signaticollis Burmeister, 1847 (Coleoptera: Scarabaeidae: Dynastinae) y observaciones sobre su biologia. Elytron. 5, 189-195.
• Nogueira, G.A.L., Rodrigues, S.R., Tiago, E.F., 2013. Biological aspects of Cyclocephala tucumana Brethes, 1904 and Cyclocephala melanocephala (Fabricius, 1775) (Coleoptera: Scarabaeidae). Biota Neotropica 13, 86-90.
• Nowinszky, L., 2004. Nocturnal illumination and night flying insects. Appl. Ecol. Envir. Res. 2, 17-52.
• Oliveira, C.M., 2007. Coró-da-soja-do-cerrado Phyllophaga capillata (Blanchard) (Coleoptera: Melolonthidae): Aspectos bioecológicos. Embrapa Cerrados Docs. 199, 11-37.
• Otsuka, K., Koshio, C., 1999. Proportion of mated females, female mating experience, and sex ratio of the osmund sawfly, Strongylogaster osmundae (Hymenoptera, Tenthredinidae). Oecologia 120, 44-49.
• Pardo-Locarno, L.C., Montoya-Lerma, J., Bellotti, A.C., Schoonhoven, A.V., 2005. Structure and composition of the white grub complex (Coleoptera: Scarabaeidae) in agroecological systems of Northern Cauca, Colombia. Florida Entomol. 88, 355-363.
• Pereira, P.R.V.S., Salvadori, J.R., 2006. Guia para identificação de corós rizófagos (Coleoptera: Scarabaeoidea: Melolonthidae) comumente encontrados em cereais de inverno, milho e soja no norte do Rio Grande do Sul. Embrapa Trigo, Comunicado técnico 204.
• Ponchel, Y., 2006. Biologie et collect de quelques dynastides. Available at: http://dynastidae.voila.net/biologie.html [accessed 25 Apr 2013].
  » http://dynastidae.voila.net/biologie.html
• Potter, D.A., Gordon, F.C., 1984. Susceptibility of Cyclocephala immaculata (Coleoptera: Scarabaeidae) eggs and immatures to heat and drought in turf grass. Envir. Entomol. 13, 794-799.
• Potter, D.A., Powell, A.J., Spicer, P.G., Williams, D.W., 1996. Cultural practices affect root-feeding white grubs (Coleoptera: Scarabaeidae) in turfgrass. J. Econ. Entomol. 89, 156-164.
• Ratcliffe, B.C., 2003. The dynastine scarab beetles of Costa Rica and Panama (Coleoptera: Scarabaeidae: Dynastinae). Bull. U. Nebraska St. Mus. 16, 41-57.
• Ratcliffe, B.C., 2008. More new species of Cyclocephala Dejean, 1821 from South America (Scarabaeidae: Dynastinae: Cyclocephalini). Coleopt. Bull. 62, 221-224.
• Ratcliffe, B.C., Cave, R.D., 2006. The dynastine scarab beetles of Honduras, Nicaragua and El Salvador (Coleoptera: Scarabaeidae: Dynastinae). Bull. U. Nebraska St. Mus. 21, 1-424.
• Ratcliffe, B.C., Cave, R.D., Cano, E.B., 2013. The dynastine scarab beetles of Mexico, Guatemala, and Belize (Coleoptera: Scarabaeidae: Dynastinae). Bull. U. Nebraska St. Mus. 27, 1-666.
• Riehs, P.J., 2006. Fenologia de algumas espécies do gênero Cyclocephala (Coleoptera, Scarabaeidae) do leste e Centro-Oeste do Paraná, Brasil. Rev. Cienc. Exat. Nat. 8, 201-223.
• Ritcher, P.O., 1966. White Grubs and Their Allies, a Study of North American Scarabaeoid Larvae. Oregon State University Monograph Series No. 4, 1-219.
• Rodrigues, S.R., Nogueira, G.A.L., Echeverria, R.R., Oliveira, V.S., 2010. Aspectos biológicos de Cyclocephala verticalis Burmeister (Coleoptera: Scarabaeidae). Neotrop. Entomol. 39, 15-18.
• Santos, V., Ávila, C.J., 2007. Aspectos bioecológicos de Cyclocephala forsteri Endrödi, 1963 (Coleoptera: Melolonthidae) no estado do Mato Grosso do Sul. Rev. Agr. 82, 298-303.
• Schwarz, M.P., 1988. Local resource enhancement and sex ratios in a primitively social bee. Nature 331, 346-348.
• Seymor, R.S., White, C.R., Gibernau, M., 2009. Endothermy of dynastine scarab beetles (Cyclocephala colasi) associated with pollination biology of a thermogenic arum lily (Philodendron solimoesense). J. Exp. Biol. 212, 2960-2968.
• Souza, T.B., Maia, A.C.D., Schlindwein, C., Albuquerque, L.S.C., Iannuzzi, L., 2014. The life of Cyclocephala celata Dechambre, 1980 (Coleoptera: Scarabaeidae: Dynastinae) in captivity with descriptions of the immature stages. J. Nat. Hist. 48, 275-283.
• Stechauner-Rohringer, R., Pardo-Locarno, L.C., 2010. Redescriptión de inmaduros, ciclo de vida, distribución e importancia agrícola de Cyclocephala lunulata Burmeister (Coleoptera: Melolonthidae: Dynastinae) en Colombia. Bol. Cient. Cent. Mus.-Mus. Hist. Nat. 14, 203-220.
• Thornhill, R., Alcock, J., 1983. The evolution of insect mating systems. Harvard University Press, Massachusetts.
• Triplehorn, C.A., Jonnson, N.F., 2011. Estudo dos insetos. Cengage Learning, São Paulo.
• Voeks, R.A., 2002. Reproductive ecology of the piassava palm (Attalea funifera) of Bahia, Brazil. J. Trop. Ecol. 18, 121-136.
• Wheller, D., 1996. The role of nourishment in oogenesis. Ann. Rev. Entomol. 41, 407-431.
• Yanega, D., 1996. Sex ratio and sex allocation in sweat bees (Hymenoptera: Halictidae). J. Kansas Entomol. Soc. 69, 98-115.
• Yanega, D., 1997. Demography and sociality in halictine bees (Hymenoptera: Halictidae). In: Choe, J.C., Crespi, B.J. (eds.). The evolution of social behavior in insects and arachinids. Cambridge University Press, Cambridge, pp. 293-315.
• Zanuncio, J.C., Didonet, J., Santos, G.P., Zanuncio, T., 1992. Determinação da idade ideal para o acasalamento de fêmeas de Podisius connexivus Bergroth, 1891 (Hemiptera: Pentatomidae) visando uma criação massal. Árvore 16, 362-367.

Publication Dates

• Publication in this collection
  Jan-Mar 2015

History

• Received
  16 July 2014
• Accepted
  03 Nov 2014