A. M. Young.
Notes on the Life Cycle and Natural History of Parides areas mylotes (Papilionidae) in Costa Rican Premontane Wet Forest.
Psyche 80:1-22, 1973.

Full text (searchable PDF, 3984K)
Durable link: http://psyche.entclub.org/80/80-001.html

The following unprocessed text is extracted from the PDF file, and is likely to be both incomplete and full of errors. Please consult the PDF file for the complete article.

PSYCHE
-
Vol. 80
March-June 1973 No. 1-2
NOTES ON THE LIFE CYCLE AND
NATURAL HISTORY OF
PARIDES ARCAS MYLOTES (PAPILIONIDAE) IN
COSTA RICAN PREMONTANE WET FOREST*
BY ALLEN M. YOUNG
Department of Biology, Lawrence University Appleton, Wisconsin 5491 I
The "Aristolochia-feeding" swallowtails of the New World tropics comprise a well-known group of butterflies famous for their roles in mimicry complexes (Brower and Brower, 1964). Although the adult stages of many congeneric species of notable genera such as Batt,us and Parides have been known for some time (Godman and Salvin, 1879-1901 ; Seitz, 1924), there is considerably less informa- tion concerning the immature stages of these butterflies. This is
particularly the case for the Central American species of Parides, one of the three genera (Battus, Parides, and the Old World Troides) of the Troidini the tribe of phannacophagous swallowtails (Ehrlich and Raven, 1965).
While the Troidini are most abundant in the Old World tropics, it is apparent that New World genera in this tribe, such as Battus and Parides, have undergone extensive speciation in Central and South America. And with the exception of a few studies such as the recent study of Battus polydmus in 'Costa Rica (Young, 197 I a) and another on the related Ornithoptera alexandrae on New Guinea (Straatman, 1971), the life cycles, behavior, and food plants of many species remain obscure. It is believed that the primarily neotropical distribution of the Aristolochiaceae (Pfeifer, 1966) is a major factor in accounting for the extensive adaptive radiation of Parities and Battus on these plants (Brower and Brower, 1964; Ehrlich and Raven, 1965).
It is the close and perhaps coevolutionary association of genera such as Parides with Aristolochia (in the Aristolochiaceae) and the co-occurrence of several sympatric congeneric species in lowland *Manuscript received by the editor March 26,1973



================================================================================

2 Psyche [March- June
tropical forests (Young, I 97 I b ) that makes these butterflies suitable candidates for the study of butterfly community structure in the tropics. In the Caribbean premontane wet forests of Costa Rica, there occur at least three species of Parities whose adults are often found together on the same flowers in forests: P. arcas nzylotes, P. childrenae, and P. sadyattes. Another subspecies of P. arcas, namely mycale, is also seen in association with these species. As an initial approach to determining the ecological factors responsible for the co-occurrence of these similar species as a functional Mullerian mimicry complex (Young, I 97 I b) , studies have been conducted on the life cycle, food plants, and other aspects of butterfly biology, for all of these species in Costa Rica. To date, the biological data for P. areas nzylotes (Bates) both in the laboratory (Young, 1972a) and field (Young, 1g71b; 1972a) has been the most extensive for these species. This paper touches upon various aspects of biology in this species not covered in the previous studies. Other reports will subsequently appear concerning the biology of the remaining species. Godman and Salvin (1879-1901) mention that P. areas mylotes is common in the Pacific and Caribbean lowlands of Central America, ranging from southern Mexico to Costa Rica. Thus the widespread geographical distribution of the butterfly throughout Central America makes it an even more attractive species to study from the standpoint of the effects of local selection pressures on natural history and life cycle.
The studies summarized here are: habitat selection, life cycle, larval food plant acceptance, and behavior of immatures and adults. Life cycle and larval food plant acceptance were examined in the laboratory, while the other studies were conducted in the field at two localities. At various times between late 1968 and mid-1970, field studies of P. areas mylotes were conducted at Finca la Selva, a region of relatively undisturbed premontane tropical wet forest (elev. about go m) located on the confluence of the Rio Puerto Viejo and Rio Sarapiqui. During the months of July and August 1972, the butter- fly was studied at Finca Tirimbina, a forest site located about 8 km west of Finca la Selva and at the basal belt transition zone (about 200 m. elev.) between montane and premontane tropical wet forest. Habitat selection was studied by observing feeding and egg-laying activities of adults at various places in the forest, both at "La Selva" and "Tirimbina". At La Selva, habitat selection was studied spo-



================================================================================

19731 Young - Parides arcas mylotes 3
radically several days each month over a 14-month period. At Tirim- bina, it was studied systematically 14 days over a two-month period. Life cycle studies consisted of the description of life stages and the estimation of egg-adult developmental time under "laboratory" conditions. These measurements were made on individuals reared on a natural food plant, and eggs were obtained in one of two basic ways. The first method was to collect eggs witnessed to be ovi- posited in the wild; this method was employed primarily in the Tirimbina studies and to a lesser extent in the earlier La Selva studies. The second method was to obtain eggs by hand-pairing newly-emerged adults, using the technique of Clarke ( 1952) for Papilio machaon, or allowing mating to occur in pairs of adults confined to plastic bags. The latter technique is useful to obtain estimates of fecundity in this species (Young, 1972a). Both methods, obtaining eggs in the wild, and mating females in the laboratory with subsequent induction of oviposition, are very successful for this species, provide large numbers of eggs for rearing studies. Combining both methods, a large number of individuals were reared from La Selva (primarily through the laboratory mating method) and a lesser number were reared from Tirimbina. The "laboratory" for the La Selva studies consisted of a well-ventilated room in an apartment in San Jose, while the ('laboratory" for the Tirimbina studies was a room in a different apartment, located about 1.5 km from the first. In both cases, air temperature usually varied between 21-23*'C and the humidity was about 45%.
The techniques for rearing immatures o1f this butterfly are given in Young ( 1972.2) for La Selva individuals, and essentially the same methods were employed for the Tirimbina studies. The larval food plant acceptance studies were conducted from individuals obtained at Tirimbina during 1972. This study consisted of offering first instar larvae immediately after hatching, in the laboratory, fresh clippings of several species of Aristolochia from various sources. The rationale was to offer separate small groups of young larvae various species of Aristolochia, including species known to be natural food plants. Larvae on each food plant were then scored for survival rate and body size. There were five species of Aristolochia that were called "novel" food plants in addition to the two natural food plant species. Two experiments were con- ducted in San Jose: in each of these, 12 larvae were reared on the natural food plant and 13 were reared on each of two "novel" food plants collected from different localities in Costa Rica. The remain- ing three food plants were tested at Lawrence University during



================================================================================

4 Psyche [March-June
September and October 1972. The three species of Aristolochia involved were already growing in a greenhouse tropical room for about two years, and the Parides eggs were transported (by air) from Costa Rica to Lawrence on September 6, 1972. Since the
natural food plant was not in culture at Lawrence, enough cuttings of it were also brought to Wisconsin to sustain the larvae through the earlier instars. At Lawrence, 10 larvae were on the natural food plant, and 8 on each of the "novel" food plants. Field studies of larval and adult behavior consisted of making repeated observations on the feeding, resting, and defensive habits of larvae in different instars, and on the oviposition behavior of adults. 'Habitat selection
Adults of both sexes of P. areas mylotes are most commonly en- countered along paths, natural clearings, swamp edges, and other exposed areas that either border forest or those which are found in the forest interior. For example, the general study site at Tirimbina where adults were most frequently seen is between the edge of forest and a small river (Fig. I). This small strip of dense secondary growth vegetation is the result of forest being cut back from the river edge for the original purpose of growing yucca and other veg- etables that form the major diet of these people. Here, the adults
fly low over dense second-growth vegetation, seldom crossing the small river, and frequently flying several meters into the shaded forest understory and canopy. Excursions into the forest were most frequently done by mated females in search of oviposition sites while males and very fresh
(presumably unmated) females generally lin- gered in the sunlight second-growth. The strip of second-growth between the forest and river is a major courtship area for this butter- fly at Tirimbina and extensive growths of the larval food plant vines are found hanging down from trees along the forest edge and grow- ing horizontally in the canopy within a few meters from the edge. A later paper (Young, et al., in prep.) will demonstrate that mated females of this species are far more prone to dispersal than either males or unmated females. In the present paper, we can say that mated females cruise along extensive tracts of cleared forest edge in search of egg-laying sites, while males and unmated females remain close to their eclosion sites. Courtship encounters are generally con- fined to low sunlight vegetation very close to where the adults emerged from their pupae. Males precede females in emergence.



================================================================================

19731 Young - Parities areas my!otes 5
Fig. 1. A major habitat of adult Puridei arcm mylotes (Bates) at Finca Tirimbina, near La Virgen, Heredia Province, Costa Rica, An adult popu- lation is found along the forest edge, and males are active in the low secondary growth vegetation between the forest and f mall river (Rio Tirimbina) to the left. August, 1972.
Thus habitat selection, which can obviously be exercised only by the adults (since eggs and larvae are relatively fixed through the oviposi- tion strategy), is molded strongly in this species by two factors: (I) establishment of optimal courtship sites by males in sunlight second-growth bordering forests or forest clearings, and (2) the response by mated females to become more prone to disperse in search for oviposition sites. Similar adult movement patterns have been seen at La Selva, and the lesser vagility of individual males was mentioned in Young (1971b). A courtship strategy in which males patrol en area of the habitat consistently day after day (Young, et al., in prep.) and mate with females as the latter emerge from their pupae, is optimal for butterflies in which males are shorter-lived than females, as is the case with Parides (Young, ig72a). But Cook et al., ( 1971 ) report a short life expectancy of about 10 days in P. anchisef



================================================================================

6 Psyche [March-June
and P. neophilus in a seasonal habitat on Trinidad where torrent rains may kill off the adults of both sexes. Although adult feeding preferences do not appear to be a major factor in dispersal patterns at Tirimbina, it is interesting to note that mimetic association with other species of Parities is most intense at nectaries at La Selva (Young, 1971b). At Tirimbina, P. arcm mylotes is the only species of this genus seen consistently at the study site, and flower specificity is not apparent. At La Selva, this butterfly as a functional component of Mullerian mimicry complexes exercise a strong preference to visit a single species of flower (Hmnelia patens) also visited by other Parities (Young, 1971 b) ; judging from the amount of time spent daily at Hamelia flowers, there appear to be very few or no other preferred adult food sources of Parides at La Selva. In the absence of the other Parides at the Tirimbina study site, adult P. areas mylotes is found on a variety of flowers, usually ranging from red to purple. Thus in the absence of strong selection pressures favoring mimetic association, and where this mimicry is potentially most effective at a food source, flower specificity may break down for Parides in habitats where the species do not co-occur on a regular basis. Similar diurnal patterns of visitation at flowers between members of a tropical Battus mimicry complex in addition to the co-occurrence of several Parides at flowers at La Selva suggest strong selection pressures resulting in convergence of feeding habits to enhance mimicry (Young, I 97 I b ; 1972b). Although courtship activity is generally limited to the sunniest hours of the morning (Young, et al., prep.), adults of both sexes and various age-classes (distinguished by the extent of wing tatter- ing) generally forage throughout the day, and they are relatively unaffected by changes in local weather conditions. Even at a mon-
tane tropical forest locality (Cuesta Angel) where a cloud forest occurs at about 1000 meters elevation, adults are seen foraging throughout the day at the bright red flowers of Impatiens sultani (Balsaminaceae - "Touch-me-nots" ) , a small herbaceous plant that is imported from Africa and that grows in large numbers. As the day becomes less bright in terms of illumination from the sun, these flowers become even more conspicuous due to increased contrast of the red coloration with the misty air; to the human observer, the flowers are more conspicuous, and perhaps the butterflies respond in a similar fashion. In both lowland and mountain localities, adult activity drops off sharply after about 4:00 P.M. When there is short succession of unusually dry days in both lowland and mountain



================================================================================

19731 Young - Parides arcas mylotes 7
localities, adults, especially males, are frequently seen visiting reced- ing mud puddles and moist patches of ground. Life cycle and developmental time
The egg (Fig. 2-A-C) is deep rusty-brown and slightly flattened at the base. The diameter is 1.1 mm and the egg is covered with an irregular thick layer of an orange-red sticky substance, which at- taches it to the leaf surface and gives the entire surface of the egg a rough appearance. This sticky substance forms thin threads which hang down from the upper half of the egg and assist in attachment (Fig, 2-A). It is not known if the sticky substance is also defensive in function, in the sense of discouraging attack by ants and other leaf-wandering predatory arthropods. The apical region of the egg darkens considerably immediately before hatching. Eggs are gen- erally laid on the ventral surface of older leaves and occasionally in the crotches of small stems and petioles (Fig. 2-C). The amount
or thickness of the sticky substance covering the eggs is apparently very variable, since other details of egg external morphology, such as deep grooves (Fig. 2-B, C) can be seen on some eggs while com- pletely obscured on others. Eggs are laid singly but usually in loose clusters of 2-5 eggs on a single leaf.
At La Selva, the natural food plant is "Aristolochia sp." (this is a new species from northeastern Costa Rica soon to be described by H. W. Pfeifer based on my collection of it during March, 1970). At Tirimbina, the natural food plant is Aristolochia constricta Griseb. Both of these species occur in lowland forest on the Carib- bean side of the central Cordillera in
Costa Rica. Pfeifer (1966)
mentions that A. constricta is a forest species found from Costa Rica to Panama, the Lesser Antilles, and probably northern South America.
The first instar is about 3.2 mm long when it hatches, and the ground color of the body is dark orange-brown. The head is shiny black. After the young larva begins to feed on leaf tissue, the body ground color becomes a deep wine red. All segments bear long tubercles of the same color as the body, but the lateral pair on the first segment are orange-white, and this color also characterizes the dorsal pairs of tubercles on segments two, seven, ten, and twelve (Fig. 2-D). The tubercles are fleshy for about one-third their length, with the apical two-thirds being stiff and bearing numerous tiny black spines (Fig. 2-D). The osmeterium is bright orange- yellow throughout larval life. By the time of the first molt, the larva is about 9 mrn long.




================================================================================

Psyche [March-June




================================================================================

The second instar is remarkably similar in appearance to the first instar, with the only major difference being a loss of the spines seen on tubercles in the previous instar. The larva (Fig. 2-E, F) retains the six rows of spines of the first instar, in addition to the shiny black head and true legs. The precise arrangement of the tubercles is very noticeable in this instar. The first four thoracic segments bear two pairs of lateral tubercles, and the uppermost pair disappears until the tenth segment where it is resumed until the twelfth seg- ment. The two pairs of lateral tubercles on these segments are not precisely in line: the tubercle of thoracic segment I are juxtaposed with those of thoracic segment 2 etc. The lateral tubercles of the thoracic segment I are considerably shorter than these tubercles on the remaining segments. The dorsal pair of tubercles on abdominal segments I and 4 are white, while the upper lateral pair of the fourth and fifth abdominal segments are also white. The highly reduced dorsal pair of the abdominal segment I I are also white. This pat- tern of tubercle arrangement and coloration is retained throughout the rest of larval life. By the second molt, the larva is about 14 mm long.
The third instar is an exact replica of the second instar except that the ground color of the body is a very deep purplish black. The third instar is shown in Fig. 2-G. By the time of the third molt, the larva is about 23 mm long. The fourth instar (Fig. 3-A) is identical to the third instar except that the skin is very shiny and reflective. It attains a length of 35 mm by the fourth molt. A dramatic change in the ground color occurs with the molt to the fifth instar (Fig. 3-B, C). The ground color is a dull, velvety purplish-brown mottled with irregular blotches8 of black, The black coloration is most extensive on the segments bearing white tubercles (Fig. 3-B, C). The white ridge along the anterior edge of the mmeterial cuff behind the head is more prominent in this instar. As this instar continues to grow, the ground color becomes even lighter in coloration as extensive velvety grayish-tan areas replace the for- merly purplish-brown areas of the body. The coloration of the dark tubercles is also variegated during the fifth instar, with each tubercle bearing lines of white in addition to the mottled coloration of the Fig. 2. Life cycle and behavior of Parides arcas mylotes (Bates). (A) dorsal view of two eggs on a leaf; note the rough surface and sticky strands on the eggs (B) single egg showing deep vertical grooves (C) sin- gle egg in crotch of stems (D) first instar, Iateral view (E) two second instar larvae (one is feeding) (F) several second instar larvae living to- gether (G) third instar, dorsal view.




================================================================================

10 Psyche [March-June




================================================================================

body ground color. By the time of pupation, the larva is about 45 mm long. The coIoratio,n of the larva remains unchanged at the time of pupation.
The pupa (Fig. 3-D) is about 25 mm long and the color pattern consists of various light shades of green and yellow. The frontal portions of the thorax and abdomen are yellow while the rest of the body is light green.
Godman and Salvin ( 1879-1901) and Seitz ( 1924) give good il- lustrations of wing color patterns of the adults (Fig. 3-E). The
single light area of the dorsal surface of the forewing in the female is cream-colored while the dorsal bands on the hindwings are osange- red. This color pattern is very consistent in both laboratory-reared and wild-caught females of P. arcas mylotes. Less stamble is the fore- wing dorsal coloration in the male within a single local population. The large spot on each forewing (Fig. 3-E) is light green but with the apical portion being cream-colored. Considerable variation is apparent in this '(two-component" spot on the dorsal surface of the male's forewing; this variability concerns the presence, absence, and size of a slecond, very small two-component spot just inside the radial cell of each forewing, and almost touching the major spot (Fig. 3-E). Similarly, there is considerable variation in the discal cell spot. Godman and Salvin ( I 879-1 go I ) mention the considerable variation in the forewing spotting pattern of male in the closely related species, P. iphidamm. Adults of both sexes of P. aTcas mylotes can be distinguished from the subspecies mycale by the presence of a thin light red marginal border of the wings in the former subspecies, while these markings are white in the latter sub- species. The red patch on the dorsal surface of the hindwings in male P, arcas mylotes is more intense than in the female) and the distribution of the coloration is very different between the sexes (Fig. 3-E). In bright sunlight, the red patches of the male's hind- wing are often iridescent, giving off a purple lustre; this is not seen in the female. The mean length o'f the forewing in the female is about 40 mm) while the same statistic of the male is about 38 mm. Thus, not only is there a striking color sexual dimorphism in this butterfly, but also a consistent wing length difference between the sexes. In the absence of crowding, laboratory-reared individuals often Fig. 3. Life cycle and behavior of Parides arcas mylotcs (Bates). (A) fourth instar) lateral view (B) fifth instar, lateral view (C) fifth instar, feeding on the tip of a young stem of Arisfolochia (D) pupa) lateral view (E) adults, female above) male below.



================================================================================

12 Psyche [March- June
bear the same wing-length as wild-caught individuals from the same locality.
The egg-adult developmental time for P. arcas 7nyZotes in the laboratory for individuals reared on Aristolochia constricts is sum- marized in Table I. In a previous study (Young, 1g72a), the egg- adult developmental time of this butterfly on Aristolochia sp. from La Selva was about 42 days.
The developmental time in that study
was measured on eggs obtained from La Selva adults. The develop- mental time for eggs obtained at Tirimbina and reared on A. con- stricta is 53 days (Table I). This difference in developmental time between the two populations is apparent in eggs, larvae, and pupae: the egg stage lasts 4 days in La Selva individuals as opposed to 6 days in Tirimbina individuals; the total larval period for La Selva in- dividuals is 17 days as opposed to 33 days in Tirinlbina individuals; the pupal stage lasts 21 days in La Selva individuals as compared to 14 days in Tirimbina individuals.
Lama2 food plant acceptance
Development from the egg stage on natural food plants is suc- cessfully completed in the laboratory (Young, I 972b ; Table I ) . When other species of Aristolochia are tested, differences in food plant acceptance by the larvae become apparent. Development is successfu1ly completed, and without a change from the Tirimbina developmental time when larvae are reared from the egg stage on Aristolochia labiata Willd. in Costa Rica. But larvae die during the first instar when offered A. veraguensis Duchr. in Costa Rica. For TABLE 1. The developmental time of Parides arcas mylotes on a natural food plant, Aristolochia consh-icta, under laboratory conditions.* INSTAR INSTAR INSTAR INSTAR INSTAR TOTAL EGG 1 2 3 4 5 PUPA EGG-ADULT
MEAN
DURATION 6 5 5 6 6 11 14 5 3
(DAYS)
k S.E. * 0.1 2 0.3 A 0.5 iz 0.3 2 0.2 0.8 zk 0.2 *Laboratory conditions consisted of confining larvae to closed plastic bags containing clippings of food plant. Physical conditions around the bags were 21-23OC and about 45'7% relative humidity. See text for further details of rearing techniques, laboratory conditions, etc.



================================================================================

19731 Young - Parides arcas mylotes 13
the rearing studies at Lawrence, all the larvae died either in the first or second instar when reared on A. ringens Vahl, A. littoralis Parodi, and A. gigantea (Mart. & Zucc.). For the groups of larvae offered these species, survivorship was 0%. Thus, in addition to the two known natural foojd plants of P. areas mylotesJ namely Aristo- lochia sp. from La Selva and A. constricts from Tirimbina, the butterfly only feeds successfully on A. labiata Willd. in Costa Rica. Behavior of adults and larvae
Observations on adult behavior are limited to the oviposition strat- egy of this species, since a later report (Young et al., in prep.) will discuss other aspects of adult behavior, most notably, the spacing patterns of males and females, and the courtship strategy. Adults of both sexes generally cruise very low over second-growth vegetation. Mated females in search of oviposition sites exhibit extreme forms of cruising behavior in two ways: (I ) they perform sudden, almost vertical darts into the canopy where Aristolochia lianas are found, and
(2) they flutter through very dense second growth within a few inches of the ground, and often being obscured from view for several minutes.