Annual Review & Research in Biology 3(1): 22-30, 2013

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Early Stages and Natural History of pausanias prasinus and M. euryleon clusoculis (, Papilionidae) from Costa Rica

Luis Ricardo Murillo-Hiller1*

1Zoocriadero de Mariposas, Escuela de Biología, Universidad de Costa Rica, 11501-2060, San José, Costa Rica.

Author’s contribution

Author LRMH did all research works for this paper.

Received 25th October 2012 st Research Article Accepted 1 January 2013 Published 6th February 2013

ABSTRACT

An extensive search for larvae was carried out in the lowland Caribbean side of Costa Rica in 2006 and 2007 to find valuable taxonomic information concerning Mimoides swallowtails. Females of Mimoides pausanias prasinus were observed laying eggs on a tree of Annona amazonica R. E. Fr. and Mimoides euryleon clusoculis on a tree of Rollinia pittieri Saff. The live material was reared at the Museum of the University of Costa Rica on their respective host-plant. Both share very similar color patterns on larvae and pupal shape. M. pausanias lasted 48 days from egg oviposition to adult emerging while M. euryleon lasted 51 days.

Keywords: Mullerian mimicry; batesian mimicry; ; M. phaon; M. microdamas; Annonaceae; Parides; Heliconius; Battus.

1. INTRODUCTION

The Mimoides Brown [1] is a neotropical group of comprised of eleven species [2]. All of them are characterized by short antennae, hairy bodies and mimetic coloration. Most of them resemble unpalatable species in the genera Parides (several ______

*Corresponding author: Email: [email protected]; Annual Review & Research in Biology, 3(1): 22-30, 2013 species), Battus (M. phaon and M. microdamas) and Heliconius (M. pausanias). They are believed to be palatable to predators and protected by batesian mimicry, by resembling coloration and behavior of their models [3].

Mimoides show very distinctive morphological and ethological characteristics, which differentiate them from all others of the tribe . DeVries [3] mentioned the peculiar rotund form of their pupae and the bearing of fleshy tubercles on the larvae and Brown [1] erected the genus according to the same reasons. The adults also are differentiated by having round hind-wings and red spots on the body and wing bases [3].

All the host plants known for this genus are in the family Annonaceae, most commonly in the genus Annona but also in the genus Guatteria and Rollinia [4]. The host plants of M. pausanias has been reported by Lamas [6] as Annona and Rollinia, whereas González and Romero [7] mentioned Annonaceae. Tyler et al. [5] informs for M. p. pausanias Annona nr. muricata as host plant in Acre (Brazil) and also includes color pictures of all instars and pupae. For Mimoides euryleon clusoculis DeVries [3] presented a brief description of the early stages and a drawing of its pupa, indicating Annona glabra and Guatteria oliviformis as host plants. For the same species Tyler et al. [5] reported Annona sp. and Constantino [8] reported Annona squamosa in Colombia. Janzen and Hallwachs [9] presented pictures of third and fifth instar larvae and pupae, feeding on Rollinia membranacea from Guanacaste, Costa Rica.

The eggs of Mimoides are greenish, with a round shape and smooth chorion, as seen on pictures presented by Tyler et al. [5]. The caterpillars present two different shapes: one bearing fleshy tubercles which mimic Parides [3,5], and the other smooth with bright yellow and bluish white lines and spots, as seen on pictures presented by Tyler et al. [5].

In Costa Rica Mimoides can be found from the sea level to 1600 m on both slopes. Of the three species present in Costa Rica, two of them (M. ilus branchus and M. euryleon clusoculis (Fig. 2) are found in many habitats, and the third one; (M. pausanias prasinus (Fig. 1) is very local and seasonal. The adults feed on flowers of various trees in the genus Cordia (Boraginaceae) and Croton (Euphorbiaceae) and bushes such as Lantana (Verbenaceae) [3]. They are active during the morning and midday. During hot days, males of these butterflies drink water from the edges of streams, rivers and roads (puddling). It is uncertain if this behavior is associated with nutrient filtering [3,5] or simply for thermoregulation by drinking cold water and expulsing it warmer.

The early stages and host plants of butterflies are important to establish relationships among closely related groups as shown by Brown [1]. Field observations, such as oviposition behavior, are needed for swallowtails butterflies because they provide important information about ancestral behavior and ecological adaptive potential [10]. By finding valuable taxonomical and ethological characteristics, it is possible to infer phylogenetic proximity and a better understanding of the ecological relationships, approaching in this way, to an effective conservation strategy of poorly known populations. It is the goal of this paper to describe the early stages and natural history features for M. euryleon clusoculis and M. pausanias prasinus to help in this regard.

2. MATERIALS AND METHODS

A butterfly sampling field trip on 11 May 2007 at the Rain Forest Aerial Tram property (450m), on the border of Braulio Carillo National Park, Limón, Costa Rica, 10º 10' 47.76" N,

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83º 55' 07.66" W, was done in order to gather biological and ethological information of butterflies. The climate in the locality is Tropical Wet Forest, Premontane Belt Transition (T- wfΔ) [11]. It is a hilly area where on sunny mornings at the sides of the Molinete river it is possible to watch males of M. pausanias prasinus puddling. Between 11:30 h and 13:30 h, a M. pausanias prasinus female was observed flying in circles at the canopy level of the host plant tree. When oviposition behavior was detected, I climbed the tree to a height of fifteen meters and collected around ten eggs. The eggs were taken to the Museo de Insectos of the University of Costa Rica, with an average room temperature of 24ºC. The hatched caterpillars were put into a plastic bag and fed with leaves of the host plant, which were brought every week from the place where the eggs were collected. The identification of the host plants were done by botanists Carlos O. Morales and Erick Villegas. From the same locality, a group of eggs of M. euryleon clusoculis were found on 21 February 2006 on a different young plant at the side of the river. These eggs were reared the same way as the M. pausanias.

The adults obtained from this study are deposited in the author’s collection. The photographs were taken with a Nikon camera model Coolpix 4500 and a reflex Canon model Rebel G.

3. RESULTS

3.1 Mimoides pausanias prasinus

Host plant: Annona amazonica R. E. Fr., a 15 m tree at the edge of a light gap on a hilly terrain.

Egg (Fig.1a): 1.2mm diameter, spherical, light-green, laid singly or in small groups of three or four eggs slightly separated, not together, on the upper side of the young leaves, always close to or in the central vein. The female butterflies glide slow, high in the canopy during hot hours searching for oviposition sites. When the tree is found, several eggs are laid on the highest young leaves. 6 days to emerge.

First instar (Fig.1b):1.7-3 mm. Head capsule round, black, stemmata black. Body predominantly colored light-green, T1 with light-green dorso-lateral scoli projected anteriorly with some setae black and others light-green and smaller light-green ventro-lateral scoli, dorsal posterior half area black, anterior light-green. T2 similar to T1 but light-green. T3 similar to T1 and T2, but also, with two dorsal scoli. Segments T3, A1, A2, A3, A7, A8, A9 with dorsal scoli. Segments from T3 to A9 with light-green lateral scoli. Segments T3, A1, A2, A3, A7, A8 dorsal area black. Time: 4 days to molt.

Second instar (Fig. 1c): 3-6.5mm. Head capsule same as first instar but bigger. Predominant body colors are black and light-yellow. T1 ventro-lateral area yellowish green bearing same color scoli, dorsal area half black and half yellowish-green with same color dorso-lateral scoli projected anteriorly with black setae. T2 dorsal area black with big yellowish-green patches. Yellowish-green dorsal small scoli and same color dorso-lateral scoli. T3 similar to T2. A1 similar to T3 but with smaller dorso-lateral scoli. A2 dorsal area black with two small dorsal scoli with black setae. Lateral area black with three yellowish-green patches and a same color small scoli. A3 similar to A2. A4 Black with a ring of big yellowish-green patches. Small lateral and dorsal yellowish-green scoli. A5 and A6 similar to A4. A7 similar to A2. A8 similar to A6. A9 yellowish-green with same color small dorsal and lateral scoli. A10 yellowish-green with no scoli. Time: 5 days to molt.

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Third instar (Fig. 1d): 6.5-16mm. Head capsule round, black, stemmata black all covered by black and gray short setae. Frons and clypeus white. T1 black with variegated pattern of yellow patches bearing two small black scoli with black setae. T2, T3 and T4 similar to T1 but without scoli. A1 to A5 black with five yellow longitudinal lines crossing laterally along the body. Three yellow lines also cross dorsally but central line is interrupted on A2, A3 and A7 and partially interrupted on A4 and A7. The two yellow lines at the sides of the central line cross from A2 to A7 but interrupted on A3, A7 and partially on A6. A8 and A9 black with yellow patches. A10 yellowish. Time: 5 days to molt.

Fourth instar (Fig. 1e): 16- 27mm. Head capsule same as third instar but bigger. No scoli in any segment. T1 to A1 black with variegated pattern of yellow patches. A2 to A7 black with one dorsal longitudinal yellow line interrupted on segments A2, A3, and A7. The dorsal yellow line is followed laterally by six more longitudinal yellow lines. Segments A8 and A9 black with yellow patches. A10 yellow. Time: 5 days to molt.

Fifth instar (Fig. 1f & 1g): 27- 43mm. Head capsule same as fourth instar but bigger. No scoli on any segment. T1 to A1 similar to fourth instar. Segments from A2 to A7 similar to fourth instar but longitudinal yellow lines interrupted as follows: dorsal line interrupted partially in A2, A4 and A6, almost absent in A3 and A7, and completely present in A5. Segments A8, A9 and A10 similar to fourth instar. Time: 6 days to molt.

Pupa (Fig. 1j): 21mm from cremaster to head horn tip. Round shape. Color polymorphic, from light-green to brown. Time: 17 days to emerge.

3.2 Mimoides euryleon clusoculis

Host plant: Rollinia pittieri Saff. a 3m tree at the edge of Molinete River.

Egg (Fig. 2a): 1.3mm diameter, spherical, light-green, laid singly or in small groups of three or four, eggs laid at the edge, ventrally and close to the petiole of mature leaves. 6 days to emerge.

First instar (Fig. 2b):1.7-3 mm. Head capsule round, black, stemmata black. Predominant body color dark brown with A4, A5 and A6 mostly white forming a “V” shape on dorsum. Segment A10 light-green color. The body bears six longitudinal lines of scoli of the same color as the body, with two at the sides of T1 projected anteriorly. Time: 4 days to molt.

Second instar (Fig. 2c): 3-6.7mm. Head capsule same as first instar but bigger. T1 mostly orange with two big scoli projected anteriorly. Posterior part of the segment black with five or six white spots around the segment. T2 with two big orange dorso-lateral scoli, two big orange dorsal warts, posteriorly on the same segment a transversal line of small orange dots and then three bigger white dots. The rest of the body presents a lateral longitudinal line of orange scoli, bigger from anterior to posterior body. Segments from T3 to A3 black with orange and white spots. A4 to A6 white. A7 and A8 black with dorsal and lateral orange scoli. A9 and A10 mostly orange with smaller dorsal and lateral scoli. Time: 5 days to molt.

Third instar (Fig. 2d): 6.7-16mm. Head capsule round, black, stemmata black, frons and clypeus white. Anterior part of T1 mostly orange with two scoli projected anteriorly. Posterior part of the segment black with five white and yellow spots around the segment. T2, T3 black with yellow and white spots. T2 and T3 with an orange dorso-lateral scoli on each side. From A1 to A5 the larva has a white dorsal line followed at each side by a thick yellow band. Form

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A1 to A7 the larva has a dorso-lateral white line followed by a yellow line. Dorsal part of A7 black with three white spots. A8 and A9 black with two and three respectively big yellow spots dorsally and small white lateral spots. A9 with an orange dorso-lateral scoli on each side. A10 mostly orange with small dorsal yellow scoli. Time: 5 days to molt.

Fourth instar (Fig. 2e): 17-31mm. Head capsule same as third instar but bigger. T1 mostly orange with two small scoli projected anteriorly. From T2 to A7 the larvae presents a white (sometimes bluish) line on dorsum. T2 and T3 with an orange dorso-lateral scoli on each side. At each side of that central line there are row of big orange yellowish spots that together forms a wide longitudinal line, followed laterally by another white (sometimes bluish) line. All these are on a black background color. Laterally presents four orange yellowish longitudinal lines. Time: 5 days to molt.

Fifth instar (Fig. 2f & 2g): 32-48mm Head capsule same as third instar but bigger. Scoli only on T1, small, black and projected anteriorly. In general it is very similar to fourth instar but all the yellow and white lines are a little bit thinner that fourth instar and therefore there it looks more black color on the body. Time: 5 days to molt (Pre-pupa Fig. 2k).

Pupa (Fig. 2j): 24mm from cremaster to head horn tip. Round shape. Color polymorphic, from light-green to brown. Time: 21 days to emerge.

Fig. 1. Early stages and adults of M. pausanias prasinus from Costa Rica: a = egg, b = first instar, c = second instar, d = third instar, e = fourth instar, f & g = fifth instar, h & i = recently emerged adult, and j = pupa

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Fig. 2. Early stages and adult of M. euryleon clusoculis from Costa Rica: a = egg, b = first instar, c = second instar, d = third instar, e = fourth instar, f & g = fifth instar, h = adult female, i = fifth instar osmeteria, j = pupa, and k = prepupa

4. DISCUSSION

All of the known host plants for Mimoides are in the family Annonaceae, particularly Annona, Guatteria and Rollinia [3,4,5,8]. However, no specific relationship has been observed between a given plant genus and a given species or species group of Mimoides. For instance, according to the compilation of host plants done by Beccaloni et al. [4] only in M. xeniades and M. thymbraeus did all the host plants recorded belong to a single genus (Annona) and even so, they are using several species of them. It may be that these two Mimoides species actually feed on other Annonaceae plants besides Annona. Many other species of Mimoides use two or more plant genera of Annonaceae as host plants.

Of the three species of Mimoides that occur in Costa Rica, M. p. prasinus is undoubtedly the least common. It can be found only on an altitudinal belt of the Caribbean side of the mountain chain complex of Costa Rica, the Cordillera Volcánica Central, Cordillera de Talamanca, Parque Internacional la Amistad and may be on the Cordillera de Tilarán and the Cordillera Volcánica de Guanacaste, between 100 and 600m above sea level. M. p. prasinus is intolerant of disturbed habitats restricting its population to national parks and natural reserves. The subspecies can be considered to be a good bio-indicator of habitat conservation level in Costa Rica, although other sub-species can be widespread and common [5]. Another limiting factor when looking for M. p. prasinus is its seasonality. As in many other members of the Leptocircini tribe, seasonality controls the population dynamics.

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Even so, M. p. prasinus can be found in low abundance all year, and higher abundance occurs during May and June. On the other hand, M. e. clusoculis is present all the year in the same locality.

It is notable that Mimoides presents two basic forms of larvae [3,5], and three basic forms of adult. The pupae are very similar in all Mimoides species and they provide little taxonomical information. The larvae of the species M. microdamas, M. ilus, and M. arianthes resemble Parides larvae [5]. The hypothesis normally accepted is that these larvae are Batesian mimics of Parides, since all the other species in the Leptocircini tribe are believed to be palatable to predators [5]. In addition, no other non-leptocircini butterflies mimic the color pattern of any species in the tribe Leptocircini, which indicates that there is not anything protective to be copied. Obviously, the larvae of these three species must be protected in some way by their coloration since they rest during daylight on the upper side of leaves. If they are not sequestering any chemical defense from the host plant then it is Batesian mimicry. A problem arises when trying to explain the color pattern of the other group of Mimoides larvae, composed of M. thymbraeus, M. euryleon, M. protodamas, M. pausanias, M. lysithous and M. phaon. All of these species share the same behavior of resting clearly exposed to predators; their coloration is completely different from any other larvae sharing their habitats. One possible explanation is that they actually are unpalatable. The larval resemblance to Parides would be explained by Müllerian mimicry and the other group of larvae (yellow striped) are just protected by aposematism. This makes sense since both groups of butterflies share the same host plants and the adults are aposematic (Table 1).

The color pattern of the adults of Mimoides resemble Parides, Battus and Heliconius. An interesting question is whether the species with the same color pattern represent lineages with a single common ancestor. In the case of the species that resemble Parides, two different larval patterns can be found: one like Parides and the other unique. If larval pattern is used to establish phylogenetic relationships between the species of Mimoides, then M. pausanias (which mimics Heliconius) would be more closely related to M. euryleon (which mimics Parides) than to M. ilus (which also mimics Parides). The only way to understand the evolutionary process of this genus is to propose a phylogenetic analysis on which several characters of adult and larvae are put together.

Table 1. Summary of Mimoides mimetic complex

Species Adult pattern Larval pattern Reference M. ariarathes Parides mimic Parides mimic [5] M. ilus Parides mimic Parides mimic [5] M. lysithous Parides mimic Parides mimic [5] M. xynias Parides mimic Undescribed - M. microdamas Battus mimic Parides mimic [5] M. phaon Battus mimic Banded larvae [5] M. pausanias Heliconius mimic Banded larvae [5] M. xeniades Parides mimic Banded larvae [12] M. thymbraeus Parides mimic Banded larvae [5] M. euryleon Parides mimic Banded larvae [3] M. protodamas Parides mimic Banded larvae [5]

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ACKNOWLEDGEMENTS

I'd like to thank Adrea González Karlsson for providing helpful comments and review of the manuscript. Also, thanks to Carlos Morales and Erick Villegas for the host plant identification. Finally, to the Rain Forest Aerial Tram of the Caribbean for allowing me to develop this research on their property.

COMPETING INTERESTS

Author has declared that no competing interests exist.

REFERENCES

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12. Méry B. Biologie d' harmodius xeniades (Lepidoptera, Papilionidae). Insectes. 1994;94(3):17-18. ______© 2013 Murillo-Hiller; This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Peer-review history: The peer review history for this paper can be accessed here: http://www.sciencedomain.org/review-history.php?iid=186&id=9&aid=903

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