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THE JOURNAL OF RESEARCH
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The Lepidoptera Research Foundation, Inc.
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William Hovanitz
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Arthur Shapiro, U.S.A.
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'j'Deceased December 17, 1985
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ISSN 0022 4324
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The Journal of Research on the Lepidoptera
25(1):1-14, 1986
Hidden Genetic Variation in Agraulis vanillae incarnata
(Nymphalidae)
Thomas E. Dimock
and
Rudolf H. T. Mattoni
111 Stevens Circle, Ventura, California 93003, U.S.A. and
9620 Heather Road, Beverly Hills, California 90210, U.S.A.
Abstract. Two culture lines of Agraulis vanillae incarnata were
established from one wild-collected female. One line was mass selected
for reduced black markings, the other for increased black markings. Both
lines were maintained through seven generations, at which time the
phenotypic differences between the lines diverged in response to selec¬
tion; a scale deformity also occurred among some individuals in the
lightly marked culture. Some genetic aspects of the variation discovered
are discussed.
Introduction
The purpose of the present work was to determine if any genes for albinic,
melanic, or immaculate Agraulis vanillae incarnata (Riley) were carried
by a field collected gravid female. These variants occur rarely in nature,
and have been described as aberrants “hewlettii” Gunder (1930),
“comstocki” Gunder (1925), “margineapertus” Gunder (1928), and
“fumosus” Gunder (1927). The probability of randomly selecting a
specimen carrying such gene(s) is admittedly small, and when it became
obvious that simple single gene variants were not likely to be expressed in
culture, the breeding program was modified to ascertain whether extreme
opposite phenotypes could be produced in parallel cultures through mass
selection. Since the color and pattern of A. vanillae throughout its range in
southern California is quite constant, this program would provide infor¬
mation on the amount of hidden genetic variation in the taxon. In A.
vanillae , which is orange with black markings on the upperside, the
approach involved selecting adults toward an all-orange upperside in one
culture line and an all-black upperside in the other. A final goal was to
cross the selected lines in order to test whether the resulting hybrids would
restore the normal phenotype, as might be expected in a complex
polygenic system (Lerner, 1954, 1958). Although the original project never
reached completion, the results obtained after seven generations are of
sufficient interest to be presented here.
2
J. Res. Lepid.
Mating and Rearing Protocol
The original female was collected on 29 October 1982 in Ventura, California.
She was confined for oviposition in a flight cage 51 x 51 x 122 cm with
several water-potted cuttings of the larval foodplant Passiflora caerulea.
The cage received afternoon sunshine plus light from a 75-watt GE Gro
and Sho Spotlight after sunset. Although courtship and mating in this
species occurs throughout the day in warm weather in natural conditions,
in this indoor breeding program these activities were limited to the latter
half of the day when the flight cage received more light.
Smaller cages for mating single pairs of adults were made from card¬
board boxes measuring 23 x 32 x 32 cm. The top and sides were cut out,
nylon netting glued over these sides, and a door cut out from the margin of
one side. When a specific pair had been chosen and mating required confir¬
mation, the caged butterflies were left in a warm room with ambient light
until noon, when they were taken out to a car. When placed on the front
seat in sunlight (or occasionally on bright but overcast skies), and with an
inside temperature of 24-30°C, matings almost always occurred. Opening
one or both car windows to provide a slight breeze helped stimulate
mating.
Ovipositing females and their progeny were left in these small cages. Cut
P. caerulea in water lasts up to two weeks, so new cuttings were added as
the older ones began to decline or were consumed, and the larvae even¬
tually found their way onto the new plants. The large flight cage was also
used as a rearing cage for broods of up to 800 larvae.
During the last instars it was necessary to clean out the denuded vine
stems and frass twice weekly. It was important to keep an adequate supply
of foodplants readily available for the larvae, as they cannibalized pupae if
these were discovered before foodplant. When most or all larvae had
pupated, the cage was cleaned and twigs with prepupae or pupae were
cropped to c. 8 cm and pushed into styrofoam mounted on a cardboard
base. Eclosing adults were examined for characteristics desired for breed¬
ing and placed into appropriate cages. Less extreme phenotypes were
saved as papered specimens. All others were liberated.
Under the above conditions, the average time for one life cycle was 45
days. Thus the entire breeding schedule described here required IOV2
months.
The Breeding Program
A pedigree of the breeding program is shown in Figure 1 . Except for those
instances where a single pair of adults was mated and their offspring
reared separately, the majority of the culture lines involved several mixed
pairs representing an extreme selected phenotype. Thus the term mass
selection is used, as multiple individuals were involved in most crosses.
The number varied in each generation, but was usually limited to the five
3
25(1) : 1-14, 1986
or ten lightest or darkest pairs. When more extreme phenotypes occurred
late in the broods, their earlier less extreme counterparts and their ova
were discarded or moved to a general mass rearing cage.
Adults from broods 1, 2, 4 and 7 showed no significant variation from
typical phenotypes. One-third of the pupae of brood 6 blackened and died,
and the remainder discarded. Many adults in brood 5 were unable to fly
properly, suggesting viability modifiers. They fluttered upside down on
the cage floor and so were not used for breeding, with the exception of a
dark female (2(5)DAD) which was mated to a slightly dark male from the
mixed brood 2mix. No G3 or G4 descendants from this mating expressed
the flight affliction. One female (3D/S DAD female #3) from the G3 of this
line showed reduced silver on the hindwing underside and was mated to a
male (3D/S D) from the dark culture (results below) . The 3D/S D male was
mated to two other females.
The hindwing upperside marginal chain pattern tended to break on the
discal side in brood BB, a characteristic we call “broken bridges”. This line
was inbred until the G3 adults were obtained (Figs. 41-42), then aban¬
doned due to lack of space.
Extreme Light and Dark Lines
Brood 8 was the major source of lightly marked adults used for selecting
the “immaculate” phenotype. This line was maintained through the
seventh generation. By the seventh generation, the upperside black spots
in the forewing interspaces M3, Cul5 Cu2 and hindwing interspaces RS, M3
and at the base of RS-Ml5 were entirely absent in most specimens. The
forewing marginal triangles and the hindwing marginal chain markings
were also greatly reduced. However, the forewing discal cell markings did
not respond to selection and remained normal in size. The gradual
development of this phenotype is shown in Figures 2-16. The results sug¬
gest that different genes or sets of genes independently control these two
sets of markings.
A selection of dark adults from the mixed brood was the source of
specimens for the dark phenotype. The remainder of specimens from the
mixed brood and those from brood 3 were discarded. After four generations
they did not exhibit facies as dark as the G2 dark mixed brood. From this
G2 brood, the darkest specimens (3DD) were bred for one generation.
Then, in the G4, offspring from the G3 female 3DD female #2 and G3 male
3D/S D were included in this brood. The dark line was then inbred until
the G7 adults eclosed. The development of this phenotype is shown in
Figures 17-28. (This line shares with the “immaculate” line the Pj female
and Gj adults in Figures 2-4.)
Variation in Undersurface Silvering
The 3D/S D male (Fig. 37), which mated three times, displayed reduc¬
tion in the silver maculation on the hindwing underside. Development of
4
J. Res. Lepid.
the silver markings was never a consideration in the selection of the light
and dark phenotypes, but the presence of two females with similar reduc¬
tions in silver markings presented an opportunity to breed this variation.
When the female 3D/S D female #1 (Fig. 38) was mated to this male, off¬
spring were as follows: 36 normal males, 52 normal females, one male with
slight silver reduction, and three females with moderate silver reduction.
When the same male was mated to female 3D/S DAD female #3 (Fig. 40),
which also displayed reduced silver markings, the offspring (26 males and
20 females) were all silvered normally. The same male was mated to a nor¬
mally silvered dark female, 3DD female #2 (Fig. 39), and their offspring
(35 males and 49 females) were also all silvered. Finally, from a mixed
brood of several pairs of adults with reduced silver markings, the following
offspring were obtained: 53 normal males, 58 normal females, and two
males and four females with reduced silver markings. The partially
unsilvered condition exhibited by several adults was usually not displayed
by their offspring, thus the heritability of the character will remain in
doubt until further controlled experiments can be performed.
Comparison of the silver markings of the G7 light phenotypes (Figs. 29-
30) with those of the dark phenotypes (Figs. 31-32) show differences in
development, especially with the “slipper-shaped” silver spot in inter¬
space RS on the hindwing. In the light phenotype the two halves of this
spot nearly coalesce; in the dark phenotype the halves have become widely
separated and smaller.
Greasy-wing
A variation having a scale deformity occurred in about 12 individuals of
the G5 generation of the “immaculate” line. These variants were called
“greasy-winged” (GW) because of their resemblance to specimens with
wings smeared by body fluids. This scale deformity affected all scales,
including those on the body. Examples of the deformity are shown
together with scales from a normal specimen in the scanning electron
microscope photographs in Figures 43-48.
The SEM photographs show that in wild type individuals the pigmented
scales differ in shape from silver scales (Fig. 42). At the highest
magnifications, the pigmented scales show spaces between the ribs, while
the silver scales in the inter-rib area appear solid. In GW individuals all
scales are reduced in size and are narrower. Further, the ultrastructure
(Figs. 45 & 48) is modified such that the inter-rib area of all scale types
appears partially filled or plugged. The effect is apparently a breakdown of
the diffractive properties of the scale surface, producing partial trans¬
parency.
The source of GW variants was the pooled brood of 4imm adults. This
brood consisted of ca. 10-15 pairs of normal adults, and their pooled G5
offspring consisted of ca. 100 normal “immaculate” phenotypes and ca. 12
GW adults (the 5GW and 6GW lines were established from these) . None of
5
25(1) :1-14, 1986
these “greasy-wings” was as extreme as those which occurred in later
broods. However, extreme “greasy-wings” did result from matings be¬
tween normal “immaculate” G6 adults.
The results of further crosses of the 4imm line to show inheritance of
GW follow:
GW x GW
(mass mating)
2
0
64
66
From above,
Normal x Normal
G6 (pair)
Normal male 19
Normal female 23
GW male 17
GW female 7
G4 offspring 100 normal: 12 GW
Normal x Normal
G5 (pair)
Normal male 12
Normal female 10
GW male 9
GW female 7
Extreme GW examples are illustrated in Figures 33 & 36. The trans¬
parency of the wings is indicated by the striped paper placed under the
wings of the specimen in Figure 34.
Data from both G5 and G6 pairings indicate the character is autosomal
and probably digenic, resulting from the interaction of paired non-linked
complementary genes. Thus a cross of two heterozygote wild types would
be expected to produce a 9+ :7 GW ratio. The pooled data give a better fit
(X2 = 1.4, df = 1, p >.25) to 9:7 than to the 3:1 ratio for a single recessive
(X2 = 10. 1 , df = 1 , p < .001 ) . F urther , if GW were due to a simple recessive,
the phenotype should have appeared in the G2 or G3 generations.
The “greasy- wing” scale deformity probably decreases fitness, and
would appear to be strongly selected against in nature. Meconium dis¬
charged from eclosing adults was not repelled by individuals with the GW
wings, but rather stuck to them and dried, sometimes causing wings to
stick together. Other specimens had lesions on the wings which oozed body
fluids at the time of wing expansion. Individuals that were able to expand
their wings successfully behaved normally; but because of the non¬
repellent nature of their wings, they would most likely experience dif¬
ficulty in humid or rainy conditions.
The cultures were terminated at the end of August 1983 for two reasons.
First, the abandoned orchard which had become completely overgrown
with Passiflora caerulea was cleared for development, eliminating the
foodplant resource, and an artificial diet was not further available.
Second, TED developed a bronchial irritation from constant exposure to
the culture, which was maintained in his living quarters.
6
J. Res. Lepid.
Discussion
The exploratory work reported here clearly shows that a significant
amount of potential genetic variation was present but masked in a single
mated female of a phenotypically constant butterfly. The variants pro¬
duced during the course of seven generations of inbreeding and selection
included individuals with substantially greater or lesser quantities of
melanin than typical A. uanillae , individuals with the scale anomaly
greasy-wings, and individuals with behavioral modifications. The genetic
systems producing these effects range from what appears to be complexes
of polygenes controlling general wing pattern density to a digenic men-
delian pair of genes for greasy-wings. Little research on inbreeding and
mass selection has been reported in the Lepidoptera (Robinson, 1971),
although inbreeding and selection is a widely used technique to determine
the amount of genetic variation in organisms (Lerner, 1954, 1958; Lewon-
tin, 1974). However, note Oliver’s, 1981, work on inbreeding depression
and some early work by Schrader, 1911. Oliver (1981) showed genetic
variability in terms of lethal equivalents in 12 lepidopteran species.
To the extent that the mated female tested is representative (a subse¬
quent abbreviated three generation experiment involving another female
produced both light and dark trending individuals, as well as the “broken
bridges” phenotypes) one might ask: why are such variants not observed
more frequently in nature? Two named aberrants “comstocki” and
“margineapertus” occasionally turn up in collections. These aberrations
closely resemble the extreme dark and light individuals selected in this
breeding program. Our results imply the genetic control of wing melanin is
not based on a few simple mendelian genes at the simultaneous recovery of
both “comstocki” and “margineapertus” types from a single individual
would be quite unlikely given the rarity of these aberrants in nature. An
albino aberrant “hewlettii” occurs very rarely in nature. The “greasy-
wing” trait, reported above, has not been reported previously. The data
reported here lead us to conclude that substantial heterozygosity for wing
character variants exist in natural populations of A. vanillae.
The magnitude of genetic variation we extracted from a single mated
individual has implications to both conservation and systematics. In con¬
servation the increasing use of captive breeding programs cannot over
emphasize the necessity of attempting to utilize a selective and breeding
scheme which maintains wild type individuals, while sequestering
variance. In systematics, the results are interesting as applied to butter¬
flies, since butterfly taxonomy at both species and subspecies levels is
based largely on wing character states which involve minor changes. The
range of variants mass selected from our single female could well represent
several different subspecies, if not species, if found fixed in natural
populations.
25(1) : 1-14, 1986
7
Acknowledgments. We are deeply indebted to Arthur M. Shapiro, Department
of Zoology, University of California at Davis (UCD), for his advice and suggestions
for the improvement of the original manuscript and for his remarks on the “greasy-
winged” condition. Rick Harris, UCD, generously provided the SEM photographs.
Our thanks to Sue Mills for proofreading the manuscript.
Literature Cited
COMSTOCK, J. A., 1927. Butterflies of California, publ. by author. Los Angeles.
334 pp.
GUNDER, J. D., 1925. Several new varieties of and aberrant Lepidoptera from
California. Ento. News 36:5-6.
_ , 1927. New transition form or “abs” and their classification. Ento.
News 38:129-138.
_ , 1928. Additionl transition forms. Can. Ento. 60:162-168.
_ , 1928b. New butterflies and sundry notes. Bull. Brooklyn Ento. Soc.
24:327-328.
LERNER, I. M., 1954. Genetic homeostasis. Wiley, New York. 134 pp.
_ , 1958. The genetic basis of selection. Wiley, New York. 298 pp.
LEWONTIN, R. C., 1974. The genetic basis of evolutionary change. Columbia
University Press, New York. 346 pp.
OLIVER, C. G., 1981. A preliminary investigation of embryonic inbreeding depres¬
sion in twelve species of Lepidoptera. Jr. Lep. Soc. 35:51-60.
ROBINSON, R., 1971. Lepidoptera genetics. Pergamon, Oxford. 687 pp.
SCHRADER, w., 1911. Inbreeding of Junonia coenia under high temperatures
through twenty-two successive generations. Pomona Jr. Zool. & Ento. 4:
673-677.
I
Pedigree of mass selection breeding project using Agraulis vanillae incarnata. Single sex symbols indicate one pair of adults
were mated to obtain progeny; double sex symbols indicate two or more pairs of adults. Numbers indicate filial generation.
Abbreviations : BB Broken Bridges; D Dark; DAD Dark and Disabled; DD Darkest Darks; D/S Diminished Silver; GW
Greasy-winged; IMM immaculate phenotype; MIX Large number of randomly mated individuals; ND Next Darkest.
25(1):1-14. 1986
9
10
J. Res. Lepid.
25(1):1-14, 1986
11
12
J. Res. Lepid.
48
14 J. Res. Lepid.
Selectively bred adults of Agraulis vanillae incarnata. Males on left, females on
right, except where noted otherwise.
Fig. 2. wild P1 female.
Figs. 3, 4. Gr
Adults bred for reduced black markings (“immaculate” phenotype):
Figs. 5, 6: G2;
Figs. 7, 8: G3;
Figs. 9, 10: G4;
Figs. 11,12: G5;
Figs. 13, 14: G6;
Figs. 15, 16: G7.
Adults bred for increased black markings (dark phenotype):
Figs. 17, 18: G2;
Figs. 19, 20: G2;
Figs. 21,22: G4;
Figs. 23, 24: G5;
Figs. 25, 26: G6;
Figs. 27, 28: Gr
Figs. 29, 30: Undersides of “immaculate” phenotypes in Figs. 15 and 16.
Figs. 31, 32: Undersides of dark phenotypes in Figs. 27 and 28.
Figs. 33, 34: “Greasy-winged” scale deformity. Male F6, female F?.
Figs. 35, 36: Undersides of Figs. 33 and 34.
Fig. 37. G3 male 3D/S. Left side ventral.
Fig. 38. G3 female 3D/S D£#1. Left side ventral.
Fig. 39. G3 female 3DD$#2. Left side ventral.
Fig. 40. G3 female 3D/S D£#3. Right side ventral.
Figs. 41, 42. G3 “broken bridges” phenotype.
Fig. 43. Scanning electron microscope photograph of the wing underside of a
normal female, brood 7imm. Magnification 160 X. Dark brown scales
at upper left, silver scales at lower right.
Fig. 44. Same as Fig. 43, magnification 640 X, dark brown scales.
Fig. 45. Same as Fig. 43, magnification 2500 X.
Fig. 46. Wing underside of a “greasy-winged” female, brood 7immGW. Magni¬
fication 160 X. Dark brown scales.
Fig. 47. Same as Fig. 46, magnification 640 X.
Fig. 48. Same as Fig. 46, magnification 2500 X.
Note: The photographs of the adult butterflies were all shot at f5.6 at 1 /250th of
a second exposure. Varying developing exposures by the automated commer¬
cial processing equipment has resulted in photographs in which the orange
ground color of the butterflies appears to vary in brightness, which in reality is
not the case. Both males and females of the “immaculate” phenotype are consis¬
tently bright orange. Dark phenotype males are slightly deeper orange, and their
females are auburn-orange.
The Journal of Research on the Lepidoptera
25(l):15-24, 1986
Electrophoretic Evidence for Speciation within the
Nominal Species Artthocharis sara Lucas (Pieridae)
Hansjurg Geiger
and
Arthur M. Shapiro
Department of Zoology, University of California, Davis, California 95616
Abstract. The taxa Anthocharis sara and A. Stella in northern California
are shown to be differentiated at the species level, using electrophoretic
genetics of both allopatric and parapatric populations. Both are also
strongly differentiated from a sample of Colorado A. julia.
Introduction
Taxonomists confronted with sets of apparently closely-related, allopat¬
ric entities are usually forced to decide on purely morphological grounds
whether to call them species or subspecies. Occasionally their judgment
can be put to test when genetic information becomes available on the
entities in question. Since the discovery of sibling speciation, it has been
generally recognized that there is no a priori correlation of morphological
differentiation and barriers to gene flow. The outcome of such genetic
tests, thus, is frequently surprising.
Anthocharis sara was described by Lucas in 1852, presumably from
somewhere near San Francisco, California. Its “subspecies” of current
usage, Stella W. H. Edwards, 1879 and julia W. H. Edwards, 1872, were
described from Nevada (type locality restricted to Marlette Peak, Carson
Range, Washoe Co., by F. M. Brown, 1973) and Colorado (type locality
restricted by Brown, loc. cit., to Beaver Creek, Park Co.). The present
study of the A. sara complex was undertaken when one of us (AMS) ob¬
served an unusual pattern of interaction in the geographic distributions of
the northern California taxa — a pattern which suggested that sara sara
and sara “stella” might in fact be full species.
Anthocharis sara sara is distributed in the Central and North Coast
Ranges, the Yolla Bollys, the Siskiyou Mountains (including the Trinity
Alps), the Cascades north of Mount Shasta, the Sierra Nevada foothills
and lower montane zone on the west slope, and in Sierra Valley on the east
slope at 1500m, 40 km N of Truckee. In northern California outside the
Sierras, it reaches at least 2000m. On the Sierran west slope, AMS has
done regular sampling at a series of stations in the South Yuba river coun¬
try since 1972. At the lowest of these, Washington (803m), only sara sara
16
J. Res. Lepid.
has been seen. At Lang Crossing (1500m) neither sara nor Stella appears to
be a permanent resident, but both have been taken with about equal fre¬
quency and no sign of intergradation. At Donner Pass (2100m), Stella is a
permanent resident and sara has been recorded three times; at Castle
Peak (2750m) sara was seen twice. At Truckee (ca. 1800m), on the east
slope, only Stella occurs. That sara occasionally intrudes at Donner Pass
was noted by Emmel and Emmel (1962, p.30), who wrote that “males
identical to typical white reakirtii were occasionally taken in fresh condi¬
tion” (“reakirtii” Edwards being a spring form of sara). The suspicious
components of this distribution are: i) the replacement of Stella by
nominate sara at high altitudes outside the Sierra; ii) the fluctuating
altitudinal range at Sierran mid-elevations, without apparent intergrada¬
tion (Table 1); and iii) the close juxtaposition of Stella with nominate sara
north of Truckee, in an apparent Great Basin habitat (juniper woodland
and meadows with a characteristic Basin butterfly fauna). We therefore
decided to seek electrophoretic evidence bearing on the probability of gene
flow and the degree of genetic differentiation among accessible pop¬
ulations. Colorado A. “sara” julia was brought into the study as an
independent geographic comparison because a sample was available; we
had no predictions concerning its status.
Materials and Methods
Samples were collected as listed in Table 2; California localities are shown in Fig.
1. All animals were transported alive and immediately stored at -70° C until elec¬
trophoresis. Only 1984 and 1985 catches were used.
The head and thorax of each individual were homogenized in 4 volumes of Tris-
HC1 buffer (0.05 M, pH 8.0). Horizontal starch gel electrophoresis was used,
following slightly modified standard procedures (Ayala et. al., 1972; Geiger, 1981).
Twenty enzymes were scored: adenylate kinase (loci AK-1 and AK-2), aldolase
(ALD), arginine kinase (APK), fumarase (FUM), glutamate -oxaloacetate trans¬
aminase (GOT-1, GOT-2), glutamate-pyruvate transaminase (GPT), glyceral-
dehyde-phosphate dehydrogenase (GAPDH), oc-glycerophosphate dehydrogenase
(dx-GPDH), indophenol oxidase (IPO), isocitrate dehydrogenase (IDH-1, IDH-2),
malate dehydrogenase (MDH-1, MDH-2), malic enzyme (ME-1), phosphoglu-
comutase (PGM), 6-phospho-gluconate dehydrogenase (6-PGD), phosphoglucose
isomerase (PGI), and pyruvate kinase (PK).
The genetic interpretation of the zymograms is based on the analysis of the pro¬
geny of parents with various phenotypes at each polymorphic locus in Pieris
brassicae (L.) (Geiger, 1982). No deviation from the pattern observed in P.
brassicae has been found in any of the three taxa investigated here. However, there
is some evidence for sex-linked inheritance of the very weakly polymorphic 6-PGD
in Stella (no polymorphism has been detected in female sara or julia). As this is
quite speculative, it has been neglected in the calculations of allelic frequencies;
this treatment does not affect any of the conclusions of this paper.
The designation of the alleles indicates the difference in the mobility of the
enzyme relative to the most frequent electromorph found in P. brassicae (index
100). An allele 95, then, codes for an enzyme that migrates 5 mm less than the P.
25(l):15-24, 1986
17
Fig. 1. Localities of Anthocharis samples studied. Abbreviations as in Table
2.
brassicae variant.
The allelic frequencies (Tables 3 and 4) have been used to calculate the statistic I
(Nei, 1972). These values have then been used to construct a dendrogram (Fig. 2)
by cluster analysis (UPGMA method, see Ferguson, 1980).
Results
The same electromorphs (treated as alleles) occur in all individuals of all
three taxa at nine of the 20 loci investigated (AK-1, AK-2, ALD, APK,
FUM, GPT, GADPH, IPO, IDH-2). At four other loci (GOT-2, oc-GPDH,
6-PGD, PK) very infrequent polymorphism is observed (frequency of the
common allele >95%, with the exception of the Donner Pass sample
( Stella ) at the 6-PGD locus, fcommon aiieie = 85%). All samples of all three
taxa share the same common allele for these loci. Variation within and/or
18
I-values
10 -i
0-9 -
0 8 -
07
Stella
/ '
/
_a>
o
O
a
o
"a>
GO
>>
Q)
£
a)
CO
o
-o
o
o
o
o
ttt— 1 99i , ;
99 , .00
i
•97 i
•91
83
Fig. 2. Dendrogram representing degree of relationship among Anthocharis
populations for which large samples are available.
between the three taxa was found at seven loci (GOT-1, IDH-1, MDH-1,
MDH-2, ME-1, PGM, PGI). The allelic frequencies at these loci are pre¬
sented in Tables 3 and 4 for all samples with at least five individuals and
for pooled samples of the three taxa. At three loci (GOT-1, MDH-1, PGI)
most alleles detected in sara with frequencies >10% are also found in
Stella (Table 3) . The two taxa show only small differences in the allelic fre¬
quencies at these three loci. This is also true for the observed variation
within the two taxa, with the exception of the Sierra Valley sample of sara.
In this sample the allele 98 is the common allele at GOT-1, with a fre¬
quency of 67% (Table 3) . Only a very low level of polymorphism is recorded
in our julia sample at these three loci. The common alleles reach very high
frequencies but appear identical with the common alleles in sara and
Stella.
The situation is different at four other loci (IDH-1, MDH-2, ME-1,
PGM) (Table 4). Statistically significant differences occur at all four loci
among the three taxa (P<1%). The IDH-1 allele 72 is found at 97% in sara
and 100% in julia but only 3% in Stella. The common allele in Stella at the
IDH-1 locus is the allele 82 that is found at 3% in sara but not in julia. At
the MDH-2 locus the allele 91 is monomorphic in all sara and Stella sam-
19
25(1) :15-24, 1986
pies, but an allele 94 is monomorphic in julia. Sara and Stella share the
same polymorphism at the ME-1 locus and in both taxa, allele 100 is the
common allele. The allele 103 that reaches 19% in sara and 9% in Stella is
the common allele in julia , with a frequency of 100%. At the PGM locus,
alleles 97, 103 and 111 are observed with frequencies >5% in sara. Only
allele 97 occurs in julia , and only at very low frequency. The three most
common alleles in Stella (90, 105, 113) are not recorded in sara and julia at
all. The common allele in julia (88) is found at low frequency in sara, and
not at all in Stella.
These data show a low degree of differentiation within the taxa, even
over substantial distances and in different climatic regimes (sara), but a
much higher degree between taxa. The quantified data are presented as I-
values in a dendogram (Fig. 2). Overall genetic differences within Stella
are small (I- values ^_0. 99). A very similar degree of divergence occurs be¬
tween the sara samples, despite their wider geographic separation. Within
sara, near-coast samples are more similar to one another than to Sierran
ones (Skelton Canyon, west slope; Sierra Valley, east), as would be pre¬
dicted. All the within- taxa comparisons are similar to values obtained
within other Pierid taxa at morphospecies level (Geiger, 1981; Geiger and
Scholl, 1982a, 1982b, 1985). The genetic differences between the taxa are
much more pronounced, and similar to those observed between morpho¬
species of Pieridae (references as above) .
The degree of heterozygosity is remarkably low in julia (Hobs =0.028,
Hexp =0.019). The values for sara (Hobs =0.091, Hexp =0.117) and stella
(Hobs =0.107, Hexp =0.120) are clearly higher.
Discussion
Low genetic differences among local populations within sara and stella
are good indicators of either contemporary or recent gene flow. The situa¬
tion is very different when these two taxa are compared, even over short
geographic distances. The Sierra Valley population of sara, which is 40 km
north of the Truckee stella population (and only about 14 km from the
nearest known stella, at Yuba Pass), is somewhat different from other sara
samples but not in any way that suggests any gene exchange with stella’, to
the contrary. At two loci (IDH-1, PGM; Table 4) the two taxa only very
infrequently have the same alleles in common, and at PGM the com¬
monest allele in each taxon is completely unknown in the other. These are
unambiguous indicators of a lack of gene flow between the taxa. As Table 1
shows, the opportunity for contact exists at least in the South Yuba River
country and probably elsewhere. We have never, however, found any
specimen intermediate between sara and stella either in the wild or in
collections, nor do we know of any permanent population (as contrasted
with the Lang Crossing case) in which both coexist.
Are sara and stella distinct species, then? In the absence of breeding-
compatibility data such a claim may seem premature, but their level of
20
J. Res. Lepid.
genetic differentiation is quite normal for Pierid morphospecies; to put it
another way, the decision to rank them as subspecies rather than species
has been based on a perceived low level of morphological differentiation,
which may not be commensurate with genomic differentiation. They are
kept apart by a narrow elevational band at mid-elevations on the Sierran
west slope in which both may colonize but neither appears capable of per¬
manent establishment. That this band is not “simply” a consequence of
habitat selection is shown by the fact that sara replaces stella in very
similar habitats and plant associations at high elevations in the Trinity
Alps (Shapiro, Palm, and Wcislo, 1981) and the Cascades north of Mount
Shasta (Ball Mountain). The nature of the exclusion from mid-elevations
on the west slope needs further study. It is duplicated with remarkable
precision in at least two other difficult groups: Phyciodes pratensis Behr/
montana Behr (Nymphalidae) and Polites sabuleti Bdv. /tecumseh Grin¬
ned (Hesperiidae) .
The genetic differences are even more pronounced between sara/stella
and Colorado julia. This julia population possesses an MDH-2 allele so far
unknown in the other taxa; at the PGM locus it shares a common
polymorphism with sara but with a different common allele. Given the
wide range of the taxon julia (Wyoming to New Mexico) and the complex
variability of the sara complex in the Rocky Mountains and Great Basin,
it is certainly premature to say too much — except that, on the face of
things, julia looks genetically like a well-defined morphospecies.
The average heterozygosity for sara and stella is typical for Pierid
species (Geiger, unpublished data) and only a little lower than for inver¬
tebrate species in general (H =0.134; Ayala, 1984). Julia is extraordinarily
homozygous, however. This could be due to sampling error (n=9),
although this value seems not to be affected by similar or even smaller
numbers in our sara and stella samples (e.g., sara, Big Bar, n=5,
Hobs 0.124; stella, Castle Peak, n=ll, Hobs =0.102). If the low value
(H0bs. =0.028) is not a sampling artifact, it could be due to (i) recent origin
of the species, (ii) a recent bottleneck for either the species or the local pop¬
ulations, (iii) founder effect, (iv) low effective population size, (v) strong
selection, or some combination of these and other factors. These matters
cannot be resolved until more information is obtained on the genetic struc¬
ture of julia populations from different parts of its range. This, in turn, is a
prerequisite for determining its precise taxonomic standing vis-a-vis not
only sara and stella but the six other named entities of the sara complex.
At the same time, re-examination of the morphological characters in the
complex and the criteria for weighting seems in order, as do compatibility
experiments and a careful comparison of both the standard and micro¬
morphology of the early stages.
Acknowledgments. We thank Francisco J. Ayala for permitting the use of his
facilities, and Oakley Shields, Adam Porter, Jane Hayes, and Steve Courtney for
21
25(l):15-24, 1986
contributing material. HJG’s work at Davis was supported by National Science
Foundation grant BSR-8306922 (Systematic Biology Program) to AMS. This
paper forms part of California Agricultural Experiment Station project CA-D*-
AZO-3994-H, “Climatic Range Limitation of Phytophagous Lepidopterans,”
AMS, Principal Investigator.
Literature Cited
AYALA, F. J., J. R. POWELL, M. L. TRACEY, C. A. MOURAO & S. PEREZ-SALAS, 1972.
Enzyme variability in the Drosophila willistonii group. IV. Genic variation in
natural populations of Drosophila willistonii. Genetics 70:113-139.
BROWN, F. M., 1973. The types of the butterflies described by William Henry
Edwards: Pieridae. Trans. Amer. Ent. Soc. 99:41, 44.
EMMEL, T. C. & J. F. EMMEL, 1962. Ecological studies of Rhopalocera in a high
Sierran community — Donner Pass, California. I. Butterfly associations and
distributional factors. J. Lepid. Soc. 16:23-44.
FERGUSON, A., 1980. Biochemical Systematics and Evolution. Blackie, Glasgow
and London.
GEIGER, H. J., 1981. Enzyme electrophoretic studies on the genetic relationships of
Pierid butterflies. I. European taxa. J. Res. Lepid. 19:181-195.
_ , 1982. Biochemisch-genetische Untersuchungen zur Systematik und
Evolution von Weisslingen des europaischen Faunengebietes. Ph.D. thesis,
University of Bern.
GEIGER, H. J. & A. SCHOLL, 1982. Enzyme electrophoretic approach to the systema¬
tics and evolution of the butterfly Euchloe ausonia. Experientia 38:927-928.
_ , 1982b. Pontia daplidice in Siideuropa — eine Gruppe von Zwei
Arten. Mitt. Schw. ent. Ges. 55:107-114.
_ , 1985. Systematics and evolution of holarctic Pierinae: an
enzyme electrophoretic approach. Experientia 41:24-29.
NEI, M., 1972. Genetic distance between populations. Am. Nat. 106:283-292.
SHAPIRO, A. M., C. A. PALM & K. L. WCISLO, 1981. The ecology and biogeography of
the butterflies of the Trinity Alps and Mount Eddy, northern California. J.
Res. Lepid. 18:69-152.
Table 1. Records of Anthocharis sara sara and A. “sara” Stella in the
South Yuba River country, northern Sierra Nevada, 1972-
1985.
Washington, Nevada Co., 803 m: sara sara only, uncommon.
Lang Crossing, Nevada Co., 1500 m: sara sara: 29.iv.74, 15.vi.74,
18. V.75, 15.vi.78; “sara” Stella: 2.vi.74, 9.vi.75, 17.iv.77, 6-8.V.84,
19. V.84.
Donner Pass, Placer-Nevada Cos., 2100 m: sara sara: 2.vii.75, 15.vi.77,
13.vii.77; “sara” Stella abundant all years.
Castle Peak, Nevada Co., 2750 m: sara sara: 30.vi.72, 8.vii.77; “sara”
Stella all years, scarce to abundant.
22 J. Res. Lepid.
Table 2. Samples of the Anthocharis sara complex used in this study.
Abbreviations are as in Fig. 1.
California sara sara:
Trinity-Siskiyou Mountains: Trinity County, Big Bar (BB), Hwy. 299, 37
km W Weaverville, 475 m, 5.V.1985 (n=5).
North Coast Ranges: Napa County: Turtle Rock (TR), Hwy. 128 near
Lake Berryessa, serpentine, 160 m, 17.iii.1984 (n=l). Solano County:
Gates Canyon (GC), Vaca Hills above Vacaville, 250-500 m, 20.iii.1984
(n=9), 4.iv.l985 (n=3).
Cascade Range: Siskiyou County: Little Shasta Meadow (LM), jet.
USFS roads 47N03 and 40N09, Ball Mountain, 2000 m, 12. vi. 1985
(n=3).
East Slope Sierra Nevada: Sierra County: Sierra Valley (SV), Hwy. 49, 4
km NE Sierraville, 8. v. 1984 (n=6).
West Slope Sierra Nevada: Mariposa County: Skelton Canyon (SK),
1200 m, 9.V.1984 (n=6). Eldorado County: 7 km S Coloma (CO), 300 m,
11. v. 1984 (n=l).
California “sara” Stella:
West Slope Sierra Nevada: Nevada County: vie. Lang Crossing (LC),
USFS road 18N18at South Yuba River, 1500 m, 8.V.1984 (n=2). Nevada +
Placer Counties: Donner Pass (DP), Hwy. 40, 2100 m, 27.V.1984 (n=3),
6.vi.l985 (n=10).
Crest, Sierra Nevada: Nevada County: Castle Peak (CP), 2700 m,
6.vi.l984 (n=10), 25.vii.1985 (n=l). Eldorado County: Red Lake Moun¬
tain (RM), Carson Pass, 3000 m, 29.vi.1985 (n=l).
East Slope Sierra Nevada: Nevada County: Truckee (TE), 1700 m,
8. v. 1984 (n = 17).
Colorado“sara” julia:
Grand County: Willow Creek Cyn., 3.vii.l984 (n=9).
number of animals investigated
25(l):15-24, 1986
23
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24
J. Res. Lepid.
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The Journal of Research on the Lepidoptera
25(l):25-29, 1986
Genetic Differentiation Between Subspecies of
Euphydryas phaeton (Nymphalidae: Nymphalinae)
A. Thomas Vawter1
and
Janet Wright2
department of Biology, Wells College, Aurora, New York 13026
2Section of Ecology and Systematics, Cornell University, Ithaca, New York 14853
Introduction
The checkerspot butterfly Euphydryas phaeton inhabits eastern North
America from the maritime provinces of Canada south to Georgia and
west to Missouri (Masters, 1968; Bauer, 1975). It is the only species of the
genus that occurs in this region, and thus, represents a biogeographic pat¬
tern different from that of its congeners in the west, which have ranges that
are generally overlapping and in some cases of limited extent. Although E.
phaeton is clearly distinct from the western species and does not show the
extreme phenotypic variation that some of them do, two subspecies have
been described. Euphydryas phaeton phaeton (Drury) occurs in the
northern portion of the species’ range where it typically inhabits marshy
meadows and similar moist habitats favored by its larval foodplant
Chelone glabra (Scrophulariaceae); E. p. ozarkae (Masters) occurs to the
south and southwest and favors drier upland forested habitats where it
reportedly feeds on Gerardia (= Aureolaria: Scrophulariaceae) (Masters,
1968). Bauer (1975) reports that E. p. ozarkae feeds on Lonicera and that
larvae from eggs deposited on Lonicera die when transferred to Chelone ,
and those from Chelone die when placed on Lonicera . He suggests that
this larval foodplant intolerance be used as a basis for dividing the taxa. D.
Bowers (personal communication) feels Bauer (1975) is in error; she
reports that E. p. ozarkae feeds naturally on Gerardia spp., although both
it and E. p. phaeton will accept Lonicera and survive on it. Furthermore,
E. p. phaeton can be reared equally well on Gerardia or Chelone , but E. p.
ozarkae does significantly better on Gerardia. Gerardia- feeding pop¬
ulations apparently also occur in upland habitats in some areas of New
York state (Shapiro, 1975).
Although these two recognizable groups of populations are most often
treated as subspecies, the marked ecological differences between them
and the apparent overlap in their geographic ranges suggests the
possibility that they may be sibling species.
Here we report the results of our study of genetic differentiation between
26 J. Res. Lepid.
E. p. ozarkae from Missouri and E. p. phaeton from central New
York.
Materials and Methods
Samples of Euphydryas phaeton were collected in the summer of 1982
from three areas in central New York and a single area in eastern Missouri.
The New York collections were made near Slaterville Springs, Tompkins
Co. (N=33); at the Oneonta Airport, Otsego Co. (N=30); and near
Milford, Otsego Co. (N=26). The Missouri collection (N=28) was made at
Merramec State Park, Franklin Co. The New York populations inhabited
wet meadows; the Missouri population inhabited mesic woodland. All
butterflies collected were stored in liquid nitrogen prior to electro¬
phoretic analysis.
Allozyme variation was assayed at 25 presumptive gene loci, following
the methods of May et. al. (1979) . Details of electrophoretic methods and a
table of electromorph frequencies are available from ATV on request.
Electromorphic frequencies were calculated from direct counts of the elec¬
trophoretic phenotypes. Nei’s (1972) measure of genetic similarity was
used to quantify genetic differentiation between populations.
Results
There are very few differences in electromorph frequencies among the 3
New York and 1 Missouri populations of E. phaeton we examined. The
average heterozygosity per locus is 0.116 + 0.019 (mean + S.E.) and the
proportion of polymorphic loci is 0.80. Log-likelihood tests for hetero¬
geneity in electromorph frequencies at each of the 25 loci (Sokal and Rohlf,
1981) illustrate the fundamental genetic similarity among the four pop¬
ulations. At only one locus (MPI) is there a heterogeneity significant at the
p=0.05 level, and one expects to find such heterogeneity at the 0.05 level
incorrectly in one in 20 such tests.
The genetic identities (Nei, 1972) further illustrate the similarities
among the populations (Table 1). The three New York populations
attributed to E. p. phaeton are somewhat more similar to each other (ave.
1=0.989) than any of them is to the Missouri population attributed to E. p.
ozarkae (ave. 1=0.967), although all four populations are quite similar.
The average genetic identity between E. p. phaeton and E. p. ozarkae that
we report here is slightly less than that reported by Brussard et al. (1985),
although their value (ave. 1=0.991) was determined by electrophoresis of
some of the same specimens. The discrepancy is due to a number of fac¬
tors. We examined more specimens, especially of E. p. phaeton, but we
used only 25 loci rather than the 28 they used. We felt on our further
analysis that we could not score all loci with confidence. We also made
some minor changes in scoring some of the loci we retained. All of these
changes are minor, and none alters the conclusions made in the earlier
work.
27
25(l):25-29, 1986
Table 1. Nei (1972) genetic identities and their standard errors (in
parentheses) between three populations of E. p. phaeton from
New York and one population of E . p. ozarkae from Missouri.
Nei’s index has a value of 1.0 for two populations that share all
alleles at the same frequency, and a value of 0.0 for two pop¬
ulations that have no alleles in common. Abbreviations for the
localities are as follows: MO = Merramec State Park, MO;
NY1 = Slaterville Springs, NY; NY2 = Oneonta, NY; NY3 =
Milford, NY.
NY1
NY2
NY3
MO
0.977(0.018)
0.968(0.024)
0.956(0.033)
NY1
—
0.990(0.004)
0.989(0.006)
NY2
—
—
0.988(0.006)
Discussion
Lack of differentiation at allozyme loci does not preclude the possibility
that the populations in question are reproductively isolated and therefore
“good” species; in the absence of other evidence that isolation exists,
however, it seems very unlikely that populations that are genetically so
similar represent separate species. Sibling species in Lepidoptera for
which data are available are clearly more different than these populations
of E. phaeton. Angevine and Brussard (1979) analyzed differentiation at
allozyme loci in populations of the satyrine butterflies Lethe eurydice and
L. appalachia that fly in dissimilar but adjacent habitats within a few
meters of each other. Although these Lethe species are morphologically
nearly indistinguishable, the genetic similarity between them was
1=0.865. Furthermore, although there were no diagnostic loci (i.e. one
population fixed for an electromorph that does not occur in the other pop¬
ulation), there were significant differences in electromorph frequencies at
5 of the 8 loci examined, and 4 of these were highly significant. Within the
genus Euphydryas , sibling species are also genetically more distant from
each other than are E. p. phaeton and E. p. ozarkae. The average genetic
identity between E. editha and its two sibling species E. chalcedona and
E. anicia is reported by Brussard et. al. (1985) to be 1=0.837, and Euphyd¬
ryas chalcedona and E. anicia, considered by those authors to be semi¬
species, have a genetic identity of 1=0.858. (Here we are following the
conservative nomenclature of Bauer (1975) rather than that of Miller and
Brown (1981), since there are no justifiable reasons to separate North
American Euphydryas into three separate genera (see Brussard et. al.,
1985) ) . Non-sibling species of butterflies are even more distinct: within the
genus Euphydryas average between-species identity is only 1=0.674
(Brussard et. al., 1985); and among European pierids it is 1=0.728
(Geiger, 1980).
28
J. Res. Lepid.
Butterfly subspecies are on the average much more similar to each other
than are sibling species. Table 2 shows genetic identities between sub¬
species in 3 genera of butterflies. All are high, most above 1=0.950; and
some (e.g., napi-bryoniae complex in Pieris) are probably not meaning¬
fully different from unity. These subspecies, therefore, though recogniz¬
able on morphological or ecological grounds, and perhaps geographically
distant from conspecific populations, are often genetically as similar as
local populations. Brittnacher et. al. (1978) suggested that the availability
of many visually discernible characters in Lepidoptera makes it easy to
find morphological differences among local populations and to elevate
some of these to races or subspecies. This may account for the low level of
genetic differentiation detected among butterfly subspecies compared to
that detected in Drosophila.
There are a number of visible phenetic or morphological differences be¬
tween E. p. phaeton and E. p. ozarkae. The latter is larger and has reduced
orange marginal markings on the ventral side of the wings. There are also
the pronounced ecological differences in habitat and foodplant choice.
Nonetheless, our analysis of allozymes reveals very little genetic difference
among the populations we have examined, even though they are more
than 1000 km apart. The lack of concordance between the ecological and
morphological traits on the one hand and the electrophoretic traits on the
other is not surprising. Singer (1982, 1983) has described variation in host
plant preference among and within populations of E. editha , and has sug¬
gested how shifts in host plant use may evolve. Under strong selection, this
evolution may occur relatively quickly. The comparatively slight allozyme
differences, however, may have resulted from much weaker selection or
none at all, and may indicate that the two lineages have been separate for
only a short time. Such would be the case if, as a growing body of evidence
now suggests (Wilson et. al., 1977; Thorpe, 1982), allozyme differences
accumulate at a stochastically constant rate and thus may serve as a
molecular evolutionary clock.
In summary, our results do not provide a definitive answer to the ques-
Table 2. Average genetic identities (Nei, 1972) between subspecies of
butterflies.
Species
Pieris napi-bryoniae
Speyeria callipe
S. coronis
S. zerene
Euphydryas editha
E. anicia
F. chalcedona
E. phaeton
0.983
0.929
0.982
0.970
0.964
0.922
0.967
I
0.992
Reference
Geiger, 1980
Brittnacher et. al., 1978
Brittnacher et. al., 1978
Brittnacher et. al., 1978
Brussard et. al., 1985
Brussard et. al., 1985
Brussard et. al., 1985
This study
29
25(l):25-29, 1986
tion of the appropriate status of E. p. phaeton and E. p. ozarkae. Overall,
there appears to have been little genetic differentiation between the two;
however, the striking behavioral and ecological differences remain.
Additional evidence from the field on the geographic distribution of the
two types of populations and laboratory studies of degrees of interfertility
would help to resolve this question.
Acknowledgments . Phil Koenig provided much useful information on E. p.
ozarkae and assisted in collecting the specimens. Robert Lacy collected the New
York samples. Deane Bowers and an anonymous reviewer offered many useful sug¬
gestions in the preparation of the manuscript. The electrophoresis was performed
at Cornell University in the laboratory of Peter F. Brussard and supported by a
grant, DEB 8116332, to him from the National Science Foundation. The adminis¬
tration of Merramec State Park, Missouri, permitted us to collect within the park;
we thank them for their cooperation.
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BRUSSARD, P. F., P. R. EHRLICH, D. D. MURPHY, B. A. WILCOX & J. E. WRIGHT, 1985.
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GEIGER, H. J., 1980. Enzyme electrophoretic studies on the genetic relationships
of Pierid butterflies (Lepidoptera: Pieridae): I. European taxa. J. Res. Lepid.
19:181-195.
MASTERS, J. H., 1968. Euphydryas phaeton in the Ozarks (Lepidoptera: Nym¬
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NEI, M., 1972. Genetic distance between populations. Amer. Natur. 106:283-292.
SHAPIRO, A. M., 1975. Butterflies of New York state. Search (New York State
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SINGER, M. C., 1982. Quantification of host preferences by manipulation of oviposi-
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_ , 1983. Determinants of multiple host use by a phytophagous insect popu¬
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SOKAL, R. & F. J. ROHLF, 1981. Biometry, 2nd ed. W. H. Freeman and Co., San
Francisco. 776 pp.
THORPE, J. P., 1982. The molecular clock hypothesis: Biochemical evolution,
genetic differentiation, and systematics. Ann. Rev. Ecol. Syst. 13:139-168.
WILSON, A. C., S. S. CARLSON & T. J. WHITE, 1977. Biochemical evolution. Ann. Rev.
Biochem. 46:573-639.
The Journal of Research on the Lepidoptera
25(l):30-38, 1986
On the Monophyly of the Macrolepidoptera, Including
a Reassessment of their Relationship to Cossoidea and
Castnioidea, and a Reassignment of Mimallonidae to
Pyraloidea
James A. Scott
60 Estes Street, Lakewood, Colorado 80226
There have been persistent reports that the closest relatives of various
Macrolepidoptera are the Cossoidea or Castnioidea. Thus Brock (1971)
claimed that butterflies evolved from Castnioidea, Bombycoidea (includ¬
ing Sphingoidea) evolved from Cossoidea, and Noctuoidea-Geometroidea
evolved from Pyraloidea. Brock’s paper is a worthwhile contribution to
certain aspects of morphology of adult Lepidoptera, but he failed to place
exact character changes on the branches of his tree, so his tree cannot be
considered either phylogenetic in any sense, or phenetic, but rather intui¬
tive (of course, every author claims that his tree represents the one and
only true phylogeny, but other workers have the right to demand proof in
terms of actual characters).
However, a detailed examination of Lepidopteran anatomy of all life
stages reveals that a very large number of characters separate the
Cossoidea and Castnioidea from the Macrolepidoptera, and that the
Macrolepidoptera form a monophyletic group. The traits are listed below
and numbered, and the numbers placed on the phylogenetic tree (Fig. 1)
where they changed in the manner described in the text. For larval traits,
see Fracker, 1915; Petersen, 1965; Forbes, 1923-1960, and Common and
Edwards, 1981. For pupae, see Mosher, 1916; Common, 1974.
No doubt there are dissenting views, and the author has no great per¬
sonal experience with moth anatomy; others should publish their
phylogenies, provided that they are supported by actual character
changes and their exact positions on the lineage, so that objective
judgments may be made about them.
Shared Derived Traits of Pyraloidea + Macrolepidoptera
(1) On the larva, the postnatal (“subprimary”) seta L3 was lost on the
prothorax, leaving only LI and L2. Nearly all other moths have LI, L2, and
L3. (2) On the larva, only one L seta is on abdomen segment 9 (other
moths have several). This trait is variable in Pyraloidea, in which some
Pyralidae subfamilies have two L setae on A9, and Pterophoridae have
many secondary setae, but Thyrididae, Carposinidae, Alucitidae, Mimal-
25(1) :30-38, 1986
31
Hesperioidea
Papilionoidea
Fig. 1 . Phylogeny of Ditrysian Lepidoptera. The numbers refer to gains, losses,
or other alterations of the characters numbered and described in text
(character 51 is in Table 1). X, possible origin of Bombycoidea-
Sphingoidea, see text.
lonidae, and most Pyralidae subfamilies have only one L seta, indicating
that one is the primitive state in the Pyraloidea. (3) On the pupal
abdomen, only segments 5-6 (joints 4-5, 5-6, 6-7) are movable (in other
Ditrysia, generally segments 3-7 move in males and 3-6 in females). (4)
On the pupal abdomen, the segments lost their special spines and the
pupa no longer protrudes from the larval burrow or cocoon (Tortricoidea,
Sesioidea, Zygaenoidea, Castnioidea, and Cossoidea have two rows of
backward-directed spines per abdomen segment used to wriggle out of the
pupation site before adult emergence). The setose pupa of many
Pterophoridae seems to be a later derivation; their long spines must have
32
J. Res. Lepid.
another purpose entirely, as they lack a cocoon. (5) Wing vein M is ves¬
tigial in the discal cell (it is present, even branched, in most other
moths). (6) Tympana evolved on the abdomen base.
Shared Derived Traits of Macrolepidoptera
(7) On the larval abdomen, setae LI and L2 became far apart; they are
close together in other moths. (8) On the pupa, maxillary palpi were
lost. (9) The adult maxillary palpi shrank to minute size (they are 3-4
segmented in Pyraloidea and earlier moths). (10) The jugal fold was lost
on the forewing base (Sharplin, 1964). (11) The CuP wing vein became
rudimentary, rather than a distinct functional vein in earlier moths. (12)
Inside the adult mesothorax, the discrimen (of Ehrlich, 1958) became
large (it is small in other moths, though moderate in size in Cos-
soidea). (13) In the adult thorax, the third metatergopleural muscle
assumed an advanced state (Sharplin, 1964). (14) The postmedian wing
lever (median wing process of Sharplin, 1964) became large (it is usually
small in other moths). In addition, all Macrolepidoptera have the heart
looped to the top of the thorax, which may be another shared derived trait,
though some microlepidoptera also have a looped heart (Hessel, 1969).
Shared Derived Traits of Noctuoidea + Bombycoidea + Sphingoidea +
Hesperioidea + Papilionoidea
(15) The tympana moved to the metathorax. The lack of additional
shared derived traits allows for the possibility that the Geometroidea is
polyphyletic, but I will leave this possibility to other workers.
Shared Derived Traits of Bombycoidea + Sphingoidea +
Hesperioidea + Papilionoidea
(16) Secondary larval setae became abundant on older larvae. (17) The
larval crochets diversified into two or three lengths (only one length in
most other moths). (18) The two adult ocelli were lost. (19) On the adult
mesothorax wall, the upper sector of the paracoxal sulcus (“precoxal
suture” of Brock) was lost (Brock’s “precoxal suture” in skippers actually
is the secondary sternopleural sulcus). (20) The tympanum was lost.
Shared Derived Traits of Sphingoidea + Hesperioidea +
Papilionoidea
(21) The cocoon was lost. (22) The adult antennae are distally enlarged
(antennae vary in more primitive moths, but filamentous antennae occur
in nearly all groups) . (23) On the adult mesothorax wall, the parepisternal
rift was lost (Brock, 1971).
25(l):30-38, 1986
Shared Derived Traits of Hesperioidea + Papilionoidea
33
(24) Eggs are upright. This is a rare condition, also possessed by Noc-
tuoidea, and a few members within other moths (some Geometroidea,
Choreutidae, Heliodinidae). Cossoidea and Castnioidea eggs have
been stated to be upright, but actually both taxa have flat eggs (I. Com¬
mon pers. comm.; Common and Edwards, 1981). (25) The larva has a
ventral neck gland used for defense, as in Noctuoidea. (26) On the pupa,
the foreleg femur is no longer visible as it is in nearly all moths. (27) The
forewing lacks an areole, and vein branches from R basad of R: in the
pupal wing (Zeuner, 1943). This areole occurs in most moths and in moths
vein R45 branches distad of Rv (28) On the adult mesothorax wall, the
anapleural cleft is fused together and undetectable (Brock, 1971). (29)
Inside the adult metathorax the furcal arms are mesally fused (Brock,
1971). (30) The adult heart is chambered where it loops to the top of the
thorax (Hessel, 1969) . The heart is looped in some moths, but only some
Cossidae have a chambered heart (other Cossidae have only a ventral un¬
chambered heart, indicating that the chamber of some Cossidae is just
convergence). (31) On the adult abdomen, the anterodorsal apodemes on
sternum 2 became minute (Brock, 1971). They are large in nearly all
moths. (32) The adult wings lost the ability to be roofed over the
abdomen.
I have not attempted to decipher the details of the phylogeny of the Dit-
rysians more primitive than Pyraloidea, except to determine that none of
them are phylogenetically close to Macrolepidoptera. The most primitive
Ditrysians, the Tineoid superfamilies, are distinguished from other Dit-
rysia by their (33) dual-rod coupling of abdomen sternum 2 with the thorax
(Brock, 1971; Heppner, 1977). In addition, the Tineoid superfamilies (34)
generally have only one row of backward-directed abdomen spines per seg¬
ment (used to wriggle out of the cocoon or burrow), whereas Cossoidea,
Castnioidea, Zygaenoidea, Sesioidea, and Tortricoidea have two rows per
segment (see character 4) . The latter five superfamilies are rather similar.
The Sesioidea apparently branched from the Ditrysian trunk after the
Cossoidea-Castnioidea-Zygaenoidea, after two wing base traits changed
(Sharplin, 1964: (35) the metabasalare lost its connection to the epister-
num or prescutum; (36) the insertion of the third metatergopleural mus¬
cle changed to an advanced condition) . Tortricoidea apparently appeared
still later after the Ditrysian trunk evolved (37) a true pointed and
crocheted cremaster (present in Tortricoidea, Pyraloidea, and Macro¬
lepidoptera), setting the stage for the appearance of Pyraloidea.
The persistent suggestions that various Macrolepidoptera evolved
independently from various primitive Ditrysia (Brock, 1971, argued that
butterflies evolved from Castnioidea, and Bombycoidea from Cossoidea)
seem wrong on both cladistic and phenetic grounds, as detailed below.
Butterflies show numerous differences fromCastnioidea and Cossoidea
34
J. Res. Lepid.
(see in particular Common, 1974), including the previous characters 1, 2,
3, 4, 5, 7, 8 (see Common and Edwards, 1981), 9, 10 (see Common and
Edwards, 1981), 11, 12, 13, 16 (secondary setae absent or rare in Cossoidea-
Castnioidea), 17, 18, 19, 21, 22 (antenna somewhat clubbed but plumose-
tipped in Castnioidea, simple to bipectinate in Cossoidea), 23, 24, 25, 27,
28, 29, 30, 31, 32, 35, 36, 37. In addition, the following traits differ between
butterflies and Cossoidea-Castnioidea: (38) the larval crochets are in a
circle or mesoseries in butterflies, in two transverse bands in Castnioidea
and many Cossoidea; (39-40) the larval head is prognathous and strongly
notched middorsally in Cossoidea-Castnioidea but not in butterflies; (41-
43) the olfactory pits on the larval head are unusual in position in
Cossoidea-Castnioidea (pit Pb is beside VI, La is far behind LI, Aa is near
the P setae, Common and Edwards, 1981), normal in butterflies; (44) on
the pupa, mandible remnants are definite bumps in Cossoidea-Castnioidea,
but are weakly developed in butterflies (the “pilifers” of Mosher,
1916); (45) on the pupa a clypeolabral sulcus occurs in Cossoidea-
Castnioidea but not in butterflies; (46) Cossoidea lack a proboscis, pre¬
sent in Castnioidea and butterflies; (47) chaetosema are absent in
Cossoidea-Castnioidea, present in butterflies; (48) the mesepimeron on
the adult thorax has a membranous division in most Cossoidea, lacking in
Castnioidea and butterflies (Brock, 1971).
Obviously, these 41 traits demonstrate a vast gap separating Cossoidea-
Castnioidea from butterflies. In fact, Cossoidea-Castnioidea are primitive
members of the suborder Ditrysia, only slightly advanced from the
Tineoidea. And the peculiar positions of the three olfactory pits (char¬
acters 41-43) on the larval head of Cossoidea-Castnioidea, (49) the lateral
position of seta AF2 on the larval head (noted by Common and Edwards,
1981 and Hinton, 1946; my Zygaenidae larvae (first instar Zygaena
trifolii) have these traits as well, except the position of pit Aa is normal),
the absence of a proboscis, and the membranous epimeron cleft of
Cossoidea surely indicate that the Cossoidea-Castnioidea-Zygaenoidea is
a derived offshoot of the moth line which could not possibly have produced
the butterflies or any other Macrolepidoptera. Evidently the superficial
butterfly-like appearance, clubbed antennae, and day-flying habits of
Castniidae have swayed the intuitive phylogenists, despite the vast
morphological gap. Nevertheless, at least 16 families of moths have day¬
flying species with colorful wings, and the microscopic details of the anten¬
nae of Castniidae and Hesperiidae are very different (Jacqueline Miller,
pers. comm.) despite their similar overall shape. Some Cossoidea have a
chambered dorsal heart as in most butterflies (character 30), but other
Cossids have the primitive ventral non-chambered heart (Hessel, 1969), so
this must be convergence.
The story regarding the relationship between Sphingidae-Bombycoidea
and Cossoidea-Castnioidea is much the same, though they are similar in
these traits: the eggs of Bomby coidea are also flat (character 24), larvae
25(1) :30-38, 1986
35
lack the neck gland (25), a cocoon is present (21), chaetosema are absent
(47), antennae are bipectinate in Bomby coidea as in some Cossoidea (22),
the anapleural cleft is a rift (28), a parepisternal rift occurs in Bom¬
by coidea (23), the metafurcal arms are more similar (29), and the sternal
apodemes are longer (31). But there still remain some 34 traits separating
Sphingoidea from Cossoidea-Castnioidea, and 32 separating Bom¬
by coidea from them. Evidently certain superficial similarities between
Bombycoidea and Cossoidea (bipectinate antennae, loss of proboscis, and
the presence of secondary setae in Limacodidae (including Megalopyginae)
and Bombycoidea, similar adult appearance of Megalopyginae and
Lasiocampidae) led intuitive phylogenists to claim a relationship, but
obviously the relationship is not genealogical.
The relationship between Cossoidea-Castnioidea and Geometroidea-
Noctuoidea shows the same wide gap, of course. In addition, Noctuoidea
have: (50) a unique MD2 seta present on T3 and A1 (present in Notodon-
tinae and other Noctuidae, Hinton, 1946) ; and Geometroidea-Noctuoidea
have tympana (characters 6, 15) . It seems probable that their tympana are
descended from that of Pyralidae, because the Geometroid tympanum is
on the first abdomen segment as in Pyralidae, and the Noctuoid tym¬
panum, which moved to the metathorax, retains a hood on the first
abdomen segment and commonly has a ventral abdominal pouch that
may have once possessed a tympanum. The Noctuoid tympanum shows
sufficient variation as to allow for the possiblility that it is descended from
the abdominal type.
The internal phylogeny of Macrolepidoptera seems straightforward ex¬
cept for the placement of Bombycoidea and Sphingoidea (see Table 1).
The Geometroidea and Noctuoidea seem the most primitive Mac¬
rolepidoptera because their larvae generally lack secondary setae and
retain one-length (uniordinal) crochets, their pupae retain the temporal
cleavage line and the visible prothorax femur, their adults retain ocelli,
tympana, and the upper sector of the paracoxal sulcus, and with Bom¬
bycoidea their adults retain the parepisternal rift and an areole. The
Geometroidea with its flat eggs, abdominal tympana (as in Pyraloidea),
and merely pectinate (not bipectinate) antenna is the more primitive of
the two.
The most advanced group of Macrolepidoptera, butterflies, shares
several derived traits with Noctuoidea: upright eggs, and a ventral larval
neck gland used for chemical defense. While the latter gland may be con¬
vergent, or lost in other Macrolepidoptera, the upright eggs of butterflies-
Noctuoidea are nearly unique (except in Heliodinidae, Choreutidae, and
some Geometridae; the Cossidae, including Cossinae, and Castniidae
always have flat eggs, I. Common, pers. comm, and Common and
Edwards, 1981). If the upright egg is genuinely co-ancestral then the
Bombycoidea-Sphingoidea branched off at point X of Figure 1. However,
using the characters and weights of Table 1, the tree of Figure 1 is the most
36
J. Res. Lepid.
Table 1. Characters of the Macrolepidoptera superfamilies. F, flat; U,
upright; +, present; absent; M, mesoseries (medial crescent);
0, oval; B, biordinal (two lengths); U, uniordinal; T, triordinal;
S, simple or filamentous; P, pectinate (two projections from
each antenna segment); B, bipectinate (four projections); C,
clubbed. In addition, traits 28-31 are derived traits of butterflies
(Hesperioidea-Papilionoidea), and 50 is a derived trait of
Noctuoidea.
a
o
T3
as
as
V
3
a
0>
a
1
a
3
O
u
i
Si
£
*3
a
4*
o
’3
a
12
a
#g
*3
*2
a>
ft
a
_o
p.
■s
•pN
Trait
W
3
5
Z
o
P5
rm
ft
00
»
E
as
Ph
o
£
16 secondary
setae
-
-
+ +
+ +
+ +
+ +
1
(+
prolegs)
(+ rarely)
17 chrochet
length
B(U)
U(B)
B
B
T(B)
T(B)
V4
18 ocelli
±.
-
-
-
-
Vi
19 upper sector
of paracoxal
sulcus
±-
-
-
-
-
y2
20 tympana
±.
±-
-
-
-
-
Vi
21 cocoon
+
+
+
-
-
-
1
(-)
22 antenna
shape
S,P
B,P,C,S
B,P
C
C
C
Vi
(P rare,
short)
23 parepisternal
rift
JL
±.
_±_
-
-
-
Vi
24 egg
F
U
F
F
u
u
1
25 ventral neck
gland on larva
-
-
-
±-
J±_
1
26 foreleg femur on
pupa visible
±.
±.
-
JL
-
-
Vi
27 areole
±.
±.
j±_
±.
-
-
1
32 wings roofed over
abdomen
±.
-
±.
-
-
Vi
38 crochet
arrangement M
47 chaetosema ±_
M M M 0 M old Vi
0 young
+ + Vi
51 temporal cleavage
line of pupa ±_ ±_ ±_ - +
1
37
25(l):30-38, 1986
parsimonious, requiring the fewest character changes of any of the possible
trees. This is partly because the Bombycoidea-Sphingoidea-butterfiles
share certain traits (crochets always bi- or triordinal, secondary setae
abundant, tympana and ocelli lost, and the upper sector of the paracoxal
sulcus lost. Because three of these traits represent losses, there is some
doubt about this parsimonious scheme, and first-instar butterflies have
primary setae, whereas first-instar Bomby coidea- Sphingoidea apparently
do not. Hopefully current and future research will add more characters to
the table to resolve this question. At the present time Figure 1 seems most
probable, which suggests that the ancestor of Bombycoidea-Sphingoidea-
butterflies was a dayflier, resulting in the loss of tympana and ocelli, and
the development of colorful wings. Sphingoidea and butterflies do share
the loss of a cocoon and a roughly similar antenna.
Eye morphology may provide relevant characters within Macrolepidop-
tera (Horridge, 1975), and demonstrates similarities between skippers and
other Macrolepidoptera. Many large nocturnal moths and skippers have a
clear zone in the eye, and skippers are similar to Bombycoidea in having
retinula cell extensions across the clear zone to the lens system (but skip¬
pers differ from Bombycoidea and others in lacking any anatomical wave
guides) and skippers resemble Agaristidae in lacking pigment in the clear
zone in daylight. Skippers and some night-adapted Macrolepidoptera
have a well-focused eye, unlike Papilionoidea (one spot on the retina
receives light focused from many ommatidia besides its own) .
It should be noted that Mimallonidae (=Lacosomidae=Perophoridae),
which have secondary setae only on the prolegs (Forbes, 1923, gives a setal
map), have been placed in Bombycoidea and Geometroidea, but various
traits place them in the Pyraloidea: abdominal setae LI and L2 adjacent;
sometimes two (or one) L setae on abdominal segment 9 (Fred Stehr, pers.
comm.); only two postnatal prothorax L setae; crochets in a circle; a well-
developed CuP vein.
Acknowledgments. I thank John B. Heppner and Ian Common for providing
some information, though their views do not necessarily correspond with Figure 1.
Clas M. Naumann kindly provided first instar Zygaenidae larvae.
Literature Cited
BROCK, J., 1971. A contribution toward an understanding of the morphology and
phylogeny of ditrysian Lepidoptera. J. Nat. Hist. 5:29-102.
COMMON, I. F. B., 1974. Lepidoptera. Chapter 36 in Insects of Australia. CSIRO.
Melbourne Univ. Press.
COMMON, I. & E. EDWARDS, 1981. The life history and early stages of Synemon
magnifica (Castniidae). J. Austral. Ent. Soc. 20:295-302.
EHRLICH, P. R., 1958. The comparative morphology, phylogeny, and higher classi¬
fication of the butterflies (Lepidoptera: Papilionoidea). Univ. Kans. Sci.
Bull. 39:305-370.
FORBES, W. T. M., 1923-1960. Lepidoptera of New York and Neighboring States.
38 J. Res. Lepid.
Parts I-IV. Memoirs 68, 274, 329, 371 of Cornell Univ. Agric. Exp. Station.
Ithaca, N.Y.
FRACKER, S., 1915. The classification of lepidopterous larvae. Contr. Ent. Labs
Univ. Ill. #43:1-169.
HEPPNER, J. B., 1977. The status of the Glyphipterigidae and a reassessment of
relationships in Yponomeutoid families and Ditrysian superfamilies. J.
Lepid. Soc. 31:124-134.
HESSEL, J. H., 1969. The comparative morphology of the dorsal vessel and acces¬
sory structures of the Lepidoptera and its phylogenetic implications. Ann.
Ent. Soc. Amer. 62:353-370.
HINTON, H. E., 1946. On the homology and nomenclature of the setae of Lepidop¬
terous larvae, with some notes on the phylogeny of the Lepidoptera. Trans.
Roy. Ent. Soc. (London) 97:1-37.
HORRIDGE, G. A., ed., 1975. The compound eye and vision of insects. Clarendon
Press, Oxford, England.
MOSHER, E., 1916. Lepidopterous pupae. A classification of the lepidoptera
based on characters of the pupa. Bull. Ill. State Lab. Nat. Hist. 12:17-159.
PETERSEN, A., 1965. Larvae of insects. Columbus, Ohio. Published by author.
SHARPLIN, J., 1964. Wing base structure in Lepidoptera. HI. Taxonomic characters.
Can. Ent. 96:943-949.
ZEUNER, F., 1943. On the venation and tracheation of the Lepidopterous fore wing.
Ann. and Mag. of Nat. Hist. 10:289-304.
The Journal of Research on the Lepidoptera
25(l):39-47, 1986
Electrophoretic Confirmation of the Species Status of
Pontia protodice and P. occidentalis (Pieridae)
Arthur M. Shapiro
and
Hansjurg Geiger
Department of Zoology, University of California, Davis, California 95616
Abstract. Electrophoretic study of sympatric and allopatric pop¬
ulations of the taxa Pontia protodice and P. occidentalis demonstrates
unequivocally that they represent closely related but independent gene
pools. Each is genetically very homogeneous over its geographic range,
strongly suggesting high levels of migration, colonization, and/or gene
flow. P. protodice is less like European P. callidice than is Californian
occidentalis , suggesting a possible phylogeny which agrees with previous
inferences from morphology and biogeography.
Introduction
The taxa Pontia (or Pieris or Synchloe) protodice Bdv. & LeC. and P.
occidentalis Reak. have posed an ongoing problem for Lepidopterists;
though Chang (1963) demonstrated morphological differences between
them and Shapiro (1976) summarized the by then copious biological and
distributional information on hand — all of which tended to support their
status as separate species — many workers, including some professionals,
have remained unconvinced and profess to be unable to classify many
specimens to one species or the other. The present study was undertaken
in the hope of further clarifying their status by comparing population sam¬
ples of both from areas of sympatry and allopatry , using electrophoresis to
quantify genomic similarities and differences. An ancillary objective was
to test the prediction that both species would show very little inter-
populational differentiation, due to their apparent pattern of colonization
and their epigamic behavior.
Materials and Methods
The sources of our samples are listed in Table 1. All animals were
transported alive and immediately stored at -70°C until electrophoresis.
Only 1984 and 1985 catches were used. All animals were determined as
protodice or occidentalis by AMS, using wing phenotype, and all wings
were saved for post-electrophoresis verification. Only one possibly
ambiguous specimen was used in the study. The head and thorax of each
40
J. Res. Lepid.
Fig. 1 . Localities for California samples. Abbreviations, numbers and makeup
by species as in Table 1.
butterfly were homogenized in 4 volumes of Tris-HCl buffer (0.05 M, pH
8.0) . We used horizontal starch gel electrophoresis, following slightly mod¬
ified standard procedures (Ayala et al., 1972; Geiger, 1981). Twenty- three
enzymes were scored: acid phosphatase (locus ACPH), adenylate kinase
(AK-1, AK-2), aldolase (ALD), arginine kinase (APK), fumarase (FUM),
glutamate-oxaloacetate transaminase (GOT-1, GOT-2), glutamate-
pyruvate transaminase (GPT), glyceraldehyde-phosphate dehydrogenase
(GAPDH), cc-glycerophasphate dehydrogenase (cd-GPDH), hexokinase
(HK), indophenol oxidase (IPO), isocitrate dehydrogenase (IDH-1, IDH-
2), malate dehydrogenase (MDH-1, MDH-2), malic enzyme (ME-1, ME-
2), phosphoglucomutase (PGM), 6-phospho-gluconate dehydrogenase
(6-PGD), phosphoglucose isomerase (PGI), and pyruvate kinase (PK).
Analysis of the progeny of parents with different phenotypes in Pieris
brassicae L. (Geiger, 1982) was the basis for interpreting zymograms of
polymorphic loci. No deviation from the pattern observed in P. brassicae
has been found in any individual investigated in this study. The dis¬
tributions of alleles are also in good accord with Hardy- Weinberg
expectations.
The most frequent allele (“common allele”) inP. brassicae was used as a
standard. This allele is designated with the index 100. Electromorphs with
different mobilities are designated in relation to this standard; an allele
25(1) :39-47, 1986 41
Table 1. Localities for samples used in this study, with notes on
sympatry.
California: Lassen County: 2.5 km S Adin, 1500 m, ll.viii.1985
(n=24)(AD), occidentalis abundant, protodice unrecorded but possible
infrequent immigrant. Siskiyou County: Ball Mountain, 2175 m,
10.viii.1985 (n=28)(BM), occidentalis only, very abundant. Sierra
County: Sierra Valley, 4 km NE Sierraville, 1500 m, 25-30. vii. 1985
(nprot =55, nocc =46)(SV), both abundant and permanently sympatric.
Placer and Nevada Counties: Donner Pass, 2100 m, 15.viii.1985 (nprot =6,
nocc =4)(DP), occidentalis common resident, protodice frequent im¬
migrant, overwintering once in 14 yr. Nevada County: Castle Peak,
2750 m, 6.vii.l985 (n=26)(CP), occidentalis only (14 yrs. of observation).
Alpine County: Leviathan Peak, 2800 m, 25.vii.1984 (nprot =2, nocc =17)
(LP), occidentalis common resident, protodice immigrant. Mono
County: nr. Mono Lake, 1800 m, 2. vii. 1985 (n ^ =17, nocc =2)(ML), pro¬
todice common, occidentalis infrequent (but commoner at higher
elevations). Kern County: Lake Isabella, 780 m, 16.viii.1985 (n=19)
(LI), protodice only. San Bernardino County: Route 38 N Onyx Sum¬
mit, elevations not available, 15.vi.1985 (n=3)(OS), protodice only.
Nevada: Churchill County: vie. Fallon, 1250 m, 13.viii.1984 (n=30),
protodice abundant, occidentalis very rare (none taken).
Florida: Broward County: vie. Davie, metropolitan Miami, 25. iv. 1984
(n=9), protodice only.
Mexico: Distrito Federal: Xochimilco-San Gregorio, 27.vi-2.vii.1984
(n=12), protodice only.
105, then, codes for an enzyme that migrates 5 mm faster than the P
brassicae variant.
The statistic I (Nei, 1972) was used to estimate the genetic similarity
between the samples over all loci. The calculated I- values for the pooled
samples of the two North American taxa plus P. callidice Hiibner have
been used to construct a dendrogram (Fig. 2) by cluster analysis (UPGMA
method, Ferguson, 1980). The Lvalues for the pooled samples are based on
only 22 loci (without ACPH) to make the data comparable to an earlier
study (Geiger and Scholl, 1985).
Results
At 16 of the 23 loci compared, protodice and occidentalis show only very
low polymorphism (fcommon allele^1 0-98), and share the same common allele
(ALD, AK-1, AK-2, APK, FUM, GADPH, GOT-2, cc-GPDH, IDH-1,
IDH-2, IPO, MDH-2, ME-1, ME-2, 6-PGD, PK) . At four other loci (GOT-
42
J. Res. Lepid.
I-value
a>
a
'■g
"o
o
)
75
CD
c
O
10,
the frequencies of all alleles are remarkably similar and show no statis¬
tically significant interpopulational differences. The situation is different
for the three remaining loci ( ACPH, HK, GPT) (Table 3) . There are two
alleles at the GPT locus which are found in both taxa but at very different
frequencies: the common allele in protodice (GPT 86) is found at very
high frequency (f >0.96) in all samples of that taxon but at much lower
frequencies (f _<_0.25) in the occidentalis samples. The allele 97 is the com¬
mon GPT allele in occidentalis (f >_0.75) and is very rarely recorded in
protodice (f ^_0.04). The genetic differences between the taxa are even
more pronounced at the HK locus, where only the allele 93 is found in pro¬
todice (f = 1.00); this allele occurs in occidentalis only at frequencies
^_0.02. At the ACPH locus each taxon is monomorphic for a different
allele.
It is important to underscore the fact that there were no heterozygous
individuals for the ACPH locus at those localities where the taxa are fre¬
quently to permanently sympatric (Donner, Sierra Valley — see Table 1).
The one possibly ambiguous individual, a female from Sierra Valley, was
electrophoretically “pure protodice” which taxon it most closely
resembled in wing phenotype. The frequencies of heterozygotes for HK
and GPT did not vary significantly between sympatric and allopatric
samples.
The very similar allelic frequencies at all loci among population samples
result_in very high I- values for the within-taxon comparisons (l0CCldentaZis =
1.00, Iprotodice >0.99) (Table 4). When the two taxa are compared the I-
value is (as expected) lower, x(I) = 0.88 ±_ 0.01.
Because HJG had already studied European P. callidice, and there has
been considerable speculation concerning its relationship to the American
taxa (Higgins and Riley, 1970; Shapiro, 1980), we compared it to our
results using the 22 loci (omitting ACPH) studied for all three taxa.
25(1) :39-47, 1986 43
Table 2. Allelic frequencies at polymorphic loci.
CTJ
B
•H
GOT-
1
MDH-
■1
PGM
PGI
CTJ
c
110
115
120
125
89
100
90
95
103
107
109
87
97
107
115 125
Sierra Valley
55
.18
.81
.02
.97
.03
.07
.90
.03
.02
.06
.84
.08
Lake Isabella
19
.05
.95
.84
.16
.03
.10
.84
.03
.03
.05
.89
.03
Mono Lake
17
.12
.85
.03
.88
.12
.03
.12
.85
.06
.91
.03
Donner Pass
6
.17
.67
.17
.92
.08
.08
.75
.17
.25
.75
cu
a
Fallon
30
.17
.82
.02
1.0
.02
.08
.80
.10
.03
.92
.05
'd
o
u
Florida
9
.28
.72
.95
.05
1 .0
1.0
o
u
Ch
Mexico
12
.13
.87
.96
.04
.04
.04
.88
.04
.08
.88
.04
all samples
153
.15
.83
.02
.95
.05
.01
.08
.86
.04
.01
.01
.06
.88
.04 .01
Ball Mtn
28
.07
.79
.14
1 .0
.07
.75
.16
.02
.04
.93
.04
CO
Ad in
24
.02
.10
.71
.17
1.0
.08
.75
.15
.02
.06
.85
.08
•U
Sierra Valley
46
.07
.79
.14
.97
.03
.01
.03
.76
.20
.01
.03
.90
.05
c
cu
T3
Castle Peak
26
.02
.81
.17
.90
.10
.02
.71
.23
.04
.04
.89
.08
O
Leviathan
17
.03
.74
.23
1.0
.09
.74
.18
.12
.82
.06
all samples
147
.01
.06
.77
.17
.97
.03
.01
.05
.75
.18
.01
.01
.05
.88
.06
Table 3. Allelic frequencies at loci with high variability between the
taxa.
n animals
ACPH
88 95
GPT
86 97
HK
93 96
Sierra Valley
55
1.0
.99 .01
1.0
Lake Isabella
19
1.0
1 .0
1.0
Mono Lake
17
1.0
.97 .03
1.0
Donner Pass
6
1.0
1 .0
1.0
at
Fallon
30
1.0
1.0
1.0
•H
XI
o
4-1
Florida
9
1.0
1.0
1.0
o
o.
Mexico
12
1.0
.96 .04
1 .0
all samples
153
1.0
.99 .01
1.0
Ball Mtn
28
1.0
.23 .77
.02 .98
Adin
24
1.0
.23 .77
.02 .98
•H
Sierra Valley
46
1.0
.13 .87
.02 .98
c
XI
Castle Peak
26
1 .0
.25 .75
1.0
u
o
o
Leviathan
17
1.0
.06 .94
1.0
all samples
147
1.0
.18 .82
.01 .99
44
J. Res. Lepid.
Occidentalis and callidice cluster at a slightly higher level than protodice.
The relationships with other species of the genus Pontia remain
unchanged.
Discussion
We had predicted a high level of genetic similarity over large distances in
these species because both are highly vagile, colonizing or “weedy” species
and because P. occidentalis is a facultative “hilltopper,” a mating
strategy which would tend to promote gene flow and prevent local ecotypic
differentiation. (For discussion of the population dynamics of P. pro¬
todice , see Shapiro, 1979; for dispersal ability of P. protodice, Shapiro,
1982 and of P. occidentalis, Shapiro, 1977; an explicit prediction was
made in Shapiro, 1984, p. 181). We were nonetheless surprised at the
extreme homogeneity of protodice over a continent-wide range (Florida,
Mexico, Nevada, California). We know that these populations are not so
homogeneous for such adaptive traits as the photoperiodic thresholds for
induction of pupal diapause, the programming and control of diapause,
hostplant adaptation and disease resistance (AMS, unpublished data).
Mexican protodice also lay smaller eggs than other populations, even
under standardized rearing conditions and on a standard diet (Shapiro, in
press). All protodice populations tested to date have been fully reproduc-
tively compatible with one another, even in such wide crosses as New York
Table 4. I-values for the comparison of all populations samples (n >6)
based on the data of 23 enzyme loci.
protodice
occidentalis
Lake Isabella
Mono Lake
Donner Pass
Fallon
Florida
Mexico
Ball Mtn
Ad in
Sierra Valley
Castle Peak
Leviathan
Sierra Valley
1.00
1.00
1.00
1.00
1.00
1.00
.89
.89
.88
.89
.87
Lake Isabella
1.00
1.00
1.00
1.00
1.00
.89
.88
.88
.89
.87
Mono Lake
1.00
1.00
1.00
1.00
.89
.89
.88
.89
.87
Donner Pass
1.00
.99
1.00
.88
.89
.88
.88
.87
Fallon
1.00
1.00
.89
.89
.88
.89
.87
Florida
1.00
.89
.89
.88
.88
.87
Mexico
.89
.89
.88
.89
.87
Ball Mtn
1.00
1.00
1.00
1.00
Ad in
1.00
1.00
1.00
Sierra Valley
1.00
1.00
Castle Peak
1.00
25(1) :39-47, 1986
45
X California or Texas, or Mexico X California; but the control of diapause
is routinely disrupted in such wide crosses, usually resulting in failure to
diapause or very rapid spontaneous termination, and much less often in
extended, lethal diapause. We have less extensive experience crossing
occidentalis populations but have found complete compatibility among
California and Colorado ones and between California and the Alaskan
subspecies nelsoni Edwards (Shapiro, 1975) which is highly incompatible
with European callidice (Shapiro, 1980). Diapause is largely unstudied in
these cases.
Vawter and Brussard (1984) found similar uniformity in the weedy,
introduced species Pieris rapae L. in eastern North America, but more
genetic diversity in the west. Populations of P. rapae in the west are dis¬
continuous, separated (except in the Central Valley of California) by
broad expanses of inhospitable terrain. The ability of P. rapae , as an
obligatorily multivoltine species, to accommodate to western climates by
altitudinal migration seems very limited in comparison to P. protodice ;
indeed, rapae is largely confined to local “mesic” pockets created by
irrigation within arid or semiarid regions, while protodice is able to
colonize throughout. This is most dramatically illustrated in central Mex¬
ico: protodice, a native species, is quite generally distributed, but the
introduced rapae is ecologically “trapped” in the floating gardens of
Xochimilco, near Mexico City, where continuous breeding is possible. It is
hardly surprising that the homogenizing effects of gene flow are more evi¬
dent in P. protodice than in P. rapae.
Vawter and Brussard argue that gene flow should be countered in
colonizing or fugitive species by genetic drift and founder effect, which
would tend to cause stochastic differences among populations. We are
examining the genetic structure of truly ephemeral populations of P. pro¬
todice (presumably resulting from colonizations by single females) in the
hope of addressing this question.
The clear genetic differences between protodice and occidentalis at
three loci are in sharp contrast to the low variation within the taxa. The
most important samples are those from Sierra Valley, where both taxa are
very abundant and apparently in stable coexistence (over 10 years, AMS
observations) and where occasional (<3%) ambiguous phenotypes are
encountered. There is absolutely no evidence for gene flow in the sympat-
ric Sierra Valley samples; the lack of ACPH heterozygotes shows that
there were no hybrids in our collections. There may indeed be
occasional, very rare spontaneous hybridization (AMS has collected one
mixed pair in copula in Donner Pass), but the electrophoretic data provide
clear confirmation that protodice and occidentalis represent separate
gene pools, corresponding to biological species. There is no evidence of
introgression (that is, the two taxa are not more similar genetically in sym-
patry than in allopatry).
It is exceedingly difficult to hybridize these two taxa spontaneously, and
46
J. Res. Lepid.
pairings can normally only be secured with a pre-excited male and a sub¬
stituted teneral allospecific female. Hand-pairings are easily achieved,
but to date the level of developmental incompatibility has been high,
resulting in dwarfing, high mortality, malformation, deficiency of the
heterogametic sex (female), and hybrid sterility. Further information on
experimental hybridization will be published elsewhere; it suffices to note
that it is fully in accord with the electrophoretic results.
Genetic differences within the group of three taxa {protodice, occiden¬
tal is, callidice) are relatively low but within the range previously reported
for closely-related species in Pieridae (Geiger, 1981; Geiger and Scholl,
1985) . This observation can be interpreted as evidence for the recency of
speciation in that group. Shapiro (1980) interpreted the group as derived
by fragmentation of the range of a widespread circumglacial steppe-
tundra entity more or less resembling the climatic adaptation of some con¬
temporary occidentalis populations. The phenotypic characteristics of
protodice are clearly derivative reductions from the full occidentalis pat¬
tern, which in the western United States is polyphenic and shows some
reduction from the nelsoni- callidice pattern. Larval and pupal characters
vary concordantly (Shapiro, unpublished data). The dendrogram thus
further supports the proposed phylogeny, which would derive occidentalis
from circumpolar proto -callidice and protodice in turn from occidentalis,
without specifying time scales. Certain central Asian taxa assigned as sub¬
species to callidice (orientalis Alph., kalora Moore, etc.) are extremely
close pheno typically to western North American occidentalis. This may
represent parallel evolution in similar climates — but then again, it may
not. Nominate callidice from the Alps and Pyrenees seems to represent the
extreme end of a long cline, physiologically as well as geographically.
We note in closing that the extreme genetic homogeneity shown by pro¬
todice and occidentalis over a large range suggests the reality of a “general
purpose genotype” associated with weediness and physiological adapt¬
ability (Baker, 1965) and the utility of these common animals as vehicles
to get a closer look at its structure.
Acknowledgments. We thank Francisco J. Ayala for permitting the use of his
facilities, and Adam Porter and Marc Minno for supplying specimens. HJG’s work
at Davis was supported by National Science Foundation grant BSR-8306922 (Sys¬
tematic Biology Program) to AMS. Field assistance was provided at various times
by Adam Porter, Doug Eby, and Cecile La Forge. This paper forms part of Cali¬
fornia Agricultural Experiment Station project CA-D*-AZO-3994-H, “Climatic
Range Limitation of Phytophagous Lepidopterans,” AMS, Principal Investigator.
The Xochimilco sample was collected with aid from a UC-MEXUS grant to AMS
and Jorge Llorente B., Universidad Nacional Autonoma de Mexico.
Literature Cited
AYALA, F. J., J. R. POWELL, M. L. TRACEY, C. A. MOURAO & S. PEREZ-SALAS, 1972.
Enzyme variability in the Drosophila willistonii group. IV. Genic variation
47
25(1) :39-47, 1986
in natural populations of Drosophila willistonii. Genetics 70:113-139.
BAKER, H. G., 1965. Characteristics and mode of origin of weeds, in H. G. Baker
and G. L. Stebbins, eds., The Genetics of Colonizing Species. Academic Press,
N.Y., pp. 147-172.
CHANG, V. C. S., 1963. Quantitative analysis of certain wing and genitalia char¬
acters of Pieris in western North America. J. Res. Lepid. 2:97-125.
FERGUSON, A., 1980. Biochemical Systematics and Evolution. Blackie, Glasgow
and London.
GEIGER, H. J., 1981. Enzyme electrophoretic studies on the genetic relationships of
Pierid butterflies. I. European taxa. J. Res. Lepid. 19:181-195.
_ , 1982. Biochemisch-genetische Untersuchungen zur Systematik und
Evolution von Weisslingen des europaischen Faunengebietes. Ph.D. thesis,
University of Bern.
GEIGER, H. J. & A. SCHOLL, 1985. Systematics and evolution of holarctic Pierinae:
an enzyme electrophoretic approach. Experientia 41:24-29.
HIGGINS, L. G. & N. D. RILEY, 1970. A Field Guide to the Butterflies of Britain and
Europe. Houghton Mifflin, Boston, p. 50.
NEI, M., 1972. Genetic distance between populations. Am. Nat. 106:283-292.
SHAPIRO, A. M., 1975. The genetics of subspecific phenotype differences in Pieris
occidentalis Reakirt and of variation in P. o. nelsoni W. H. Edwards
(Pieridae). J. Res. Lepid. 14:61-83.
_ , 1976. The biological status of Nearctic taxa in the Pieris protodice-
occidentalis group (Pieridae). J. Lep. Soc. 30:289-300.
_ , 1977. Apparent long-distance dispersal by Pieris occidentalis (Pieridae).
J. Lep. Soc. 31:202-203.
_ , 1979. Weather and the lability of breeding populations of the check¬
ered white, Pieris protodice Bdv. & LeC. (Pieridae). J. Res. Lepid. 17:1-23.
_ , 1980. Genetic incompatibility between Pieris callidice and P. occiden¬
talis nelsoni : differentiation within a periglacial relict complex. Can. Ent.
112:463-468.
_ , 1982. A new elevational record for Pirns protodice in California (Lepi-
doptera: Pieridae). Pan-Pac. Ent. 58:162.
_ , 1984. Polyphenism, phyletic evolution, and the structure of the Pierid
genome. J. Res. Lepid. 23:177-195.
_ , in press, r and K selection at various taxonomic levels in the pierine
butterflies of North and South America, in F. Taylor and R. Karban, eds.,
Evolution of Insect Life Histories. Springer-Verlag, Berlin, pp.
VAWTER, A. T. & P. F. BRUSSARD, 1984. Allozyme variation in a colonizing species:
the cabbage butterfly Pieris rapae (Pieridae). J. Res. Lepid. 22:204-216.
The Journal of Research on the Lepidoptera
25(1):48-51, 1986
Susceptibility of Eggs and First-Instar Larvae of
Callosamia promethea and Antheraea polyphemus
to Malathion1
Thomas A. Miller, William J. Cooper2 and Jerry W. Highfill3
US Army Medical Bioengineering R&D Laboratory, Fort Detrick, Maryland 21701
Abstract. Susceptibility levels to malathion water emulsions are
established for Callosamia promethea (Drury) and Antheraea poly¬
phemus (Cramer): C. promethea eggs, LC50 = 0.1 mg/ml, probit = 3.3 +
0.9 (log cone); C. promethea lst-instar larvae, LC50 = 0.01 mg/ml, probit
= 11.3 + 2.9 (log cone); A. polyphemus eggs, LC50 between 15.6 and 31.2
mg/ml; A. polyphemus lst-instar larvae, LC50 = 0.06 mg/ml; probit = 9.9
+ 4.1 (log cone); C. promethea embryos, LC50 = 248 mg/ml, probit = -2.3
+ 3.0 (log cone).
Introduction
Giant silkworm moths, such as Callosamia promethea (Drury) and
Antheraea polyphemus (Cramer), used for research purposes, are reared
on foliage obtained in agricultural or domestic situations where organo-
phosphate insecticides may be applied or stored. Information is not avail¬
able on the susceptibility of the early stages of these giant silkworm moths
to foliar applications or organophosophate insecticides. To estimate the
susceptibility of these insects to natural, potentially contaminated
foliage, we determined the laboratory susceptibility of eggs and lst-instar
larvae of C. promethea and A. polyphemus to malathion, 0,0-dimethyl
phosphorodithioate of diethyl mercaptosuccinate, a representative,
commonly-used organosphophate material. These estimates of suscepti¬
bility are based on laboratory testing procedures, and do not account for
field conditions (e.g., pH, temperature, humidity, residue age) that might
alter the effective toxicity of the malathion.
Materials and Methods
Test insects were obtained from colonies of C. promethea and A.
polyphemus reared in sleeve cages on wild cherry ( Prunus serotina ) or
1Lepidoptera: Saturniidae. This research was not supported by public funds. The opinions
contained herein are those of the authors and should not be construed as official or reflecting
the views of the Department of the Army.
2Present address: Drinking Water Research Center, Florida International University,
Miami, FL 33199.
3Present address: USEPA Health Effects Research Laboratory, Research Triangle Park, NC
27711.
25(1):48-51, 1986
49
various maples (. Acer spp.) for 10-12 generations. Ortho Malathion 50
Insect SprayR (Chevron Chemical Company Ortho Division, San Fran¬
cisco, CA 94119, EPA Reg. No. 239-739-AC) an emulsifiable concentrate
containing 50 percent actual malathion by weight (521 mg/ml), was used
for all testing. The appropriate quantity of emulsifiable concentrate was
added to water with a volumetric pipet to make a stock emulsion. The
stock emulsion was diluted with water, with constant stirring of stock and
dilutions, to produce the test concentrations. For larvicide tests,
individual hostplant leaves were dipped in test emulsions for 30 seconds
and allowed to air dry. Control leaves were dried separately after being
dipped only in water. Unfed, lst-instar larvae (<24 hours old) were placed
in random sequence on the treated and control leaves and held in plastic
cups and covered with facial tissues for 48 hours before recording mor¬
tality. For ovicide tests, egg masses (<48 hours old) were dipped in ran¬
dom sequence in test emulsions for 30 seconds, then allowed to air dry.
Control egg masses were dipped in water only, then allowed to air dry
separately. Mortality of treated eggs was determined as those that failed
to hatch after all control eggs hatched. Embryos of C. promethea were tested
at high concentrations of malathion (up to 500 mg/ml) to determine the
existence of a concentration- mortality relationship. The percentage of
embryo mortality rather than the hatch failure was the measured
criterion. Mortality data on embryos, eggs, and larvae were subjected to
probit analysis using a computer program package described by Barr, et
al. (1976).
Results and Discussion
The label recommended concentration for spray application of mala¬
thion water emulsion to fruit and ornamental foliage is 12.0 mg Al/ml.
Table 1 shows that both eggs and lst-instar larvae of C. promethea and
lst-instar larvae of A. polyphemus were highly susceptible to recommended
doses. The concentration-mortality relationships for C. promethea eggs
and lst-instar larvae are shown in Figures 1 and 2. Eggs of A. polyphemus
were not susceptible at label concentrations; those exposed to concen¬
trations of up to 15.6 mg/ml showed no ovicidal effects, while those
exposed to concentrations of 31.2 mg/ml and above showed no hatch. No
concentration- mortality relationship was established for A. polyphemus
eggs. The concentration-mortality relationship applicable to A. poly¬
phemus lst-instar larvae is shown in Figure 3. Embryos of C. promethea
were not susceptible to label concentration of malathion water emulsion
(Table 1). However, toxicity to embryos was observed at the higher con¬
centrations used in initial range finding. In some of these tests, fully-
formed larvae were present in the eggs, but did not hatch. In C. promethea
the developing dark larva imparts a gray hue to the otherwise white egg.
The presence of larvae in the “gray” eggs was confirmed by dissection.
50 J. Res. Lepid.
Table 1. Malathion susceptibility of eggs and larvae of Callosamia pro-
methea and Antheraea polyphemus.1
Stage
Tested
Number
Tested
LC50
LC90
Relative
Susceptibility2
at LC50
Callosamia promethea
Embryos
450
248
659
0.05
Eggs
650
0.1
0.36
120
lst-Instar
Larvae
380
0.01
0.02
1200
Antheraea polyphemus
Eggs3
120
>15.6
>15.6
>0.77
lst-Instar
Larvae
280
0.06
0.13
200
1all values in mg/ml
2label concentration/lethal concentration (LC50)
3no ovicidal effects observed at 15.6 mg/ml
This condition was not observed in ovicide tests with A. polyphemus
because the light yellow larvae are not visible through the tan egg shells
and no dissections were performed. Tests conducted with high concen¬
trations of malathion (Figure 4) demonstrated that a concentration-
mortality relationship existed.
Mortality preceding eclosion of eggs has been observed in many lepidop-
terans in connection with exposure to ovicides, but the phenomenon in
general is poorly understood (Smith & Salkeld, 1966). Potter, et al. (1957)
reported that high concentrations of TEPP (tetraethyl pyrophosphate)
caused mortality in eggs of Pieris hrassicae Linnaeus; older eggs being
considerably more susceptible than younger ones. They concluded that
toxicity due to organophosphate exposure appears to involve cholines¬
terase inhibition at some stage of embryonic development. The C. pro-
methea eggs we tested were less than 48 hours old. For those exposed to
malathion water emulsion at 0.01 mg/ml all of the embryos developed, but
only 50 percent hatched; for those exposed to 248 mg/ml only 50 percent of
the embryos developed and none hatched.
These studies establish baseline susceptibility of immature stages of C.
promethea and A. polyphemus to malathion water emulsions, and
demonstrate that the immature stages are susceptible at recommended
dosages. The particular hazard presented by malathion, or other more
toxic or more persistent organosphosphate materials, depends on other
variables, such as pH, temperature, humidity, and residue age, not
included in these studies.
PERCENT MORTALITY PERCENT MORTALITY
25(0:48-51, 1986
51
MALATHION (mg/ml) MALAT H IO N(mg/ ml)
Figs. 1-4. Susceptibility of Giant Silkworm Moth Eggs and Larvae to Malathion
Water Emulsion: 1. Callosamia promethea Eggs; 2. Callosamia pro-
methea Ist-lnstar Larvae; 3. Antheraea polyphemus Ist-lnstar Lar¬
vae; 4. Callosamia promethea embryos.
Literature Cited
BARR, A. J., J. H. GOODNIGHT, J. P. SAUL & J. T. HELWIG, 1976. A User's Guide to SAS
76. SAS Institute, Inc., Raleigh, NC pp. 206-211.
POTTER, C., K. A. LORD, J. KENTON, E. H. SALKELD & D. V. HOLBROOK, 1957. Embryonic
Development and Esterase Activity of Eggs of Pieris brassicae in Relation to
TEPP Poisoning. Ann. Appl. Biol. 45:361-375.
SMITH, E. H. & E. H. SALKELD, 1966. The Use and Action of Ovicides. Ann. Rev.
Entomol. 11:331-368.
PROBITS PROBITS
The Journal of Research on the Lepidoptera
25(l):52-62, 1986
Pupal Mortality in the Bay Checkerspot Butterfly
(Lepidoptera: Nymphalidae)
Raymond R. White
788 Mayview Avenue, Palo Alto, California 94303
Abstract. Mortality for pupae of Euphydryas editha bayensis (Lepi¬
doptera: Nymphalidae) placed in the field ranged from 53 to 89%. Preda¬
tion and cold weather during the period of pupation were the major
mortality factors. Mortality during this stage is high enough to affect
total numbers of adults and other life stages and variable enough to affect
the population dynamics of these butterflies. Studies of these and other
holometabolous insect species should include estimates of pupal
mortality.
Introduction
Few complete life tables have been published for natural populations of
butterflies (see Dempster, 1983). This is partly because at least one life
stage of these holometabolous insects is difficult or impossible to observe
in the field. For example, Euphydryas editha bayensis Sternitzky (1937)
(the Bay Checkerspot butterfly) is among the most thoroughly studied
insects, but only its adult stage is easily observable. Eggs and prediapause
larvae have only recently been found in numbers, and diapausing larvae
remain essentially a “black box” to us. Many post-diapause larval sam¬
ples have been collected and some data on parasitoid rates have been
published (Ehrlich, 1965; White, 1973 and Stamp, 1984). Pupae are
almost never seen.
Prior to this study the only information on pupal mortality in Euphydryas
editha was Singer’s observation that several out of 20 pupae placed out at
Jasper Ridge were eaten and the wooden tongue depressors used to mark
them had been chewed on by rodents (Singer, 1971).
Life table data for butterfly populations that have been published show
pupal mortalities ranging from 0 to 100%, but averaging around 60%
(Table 1). Most of the pupal mortality identified was due to predation.
With this background I did an experiment designed to quantify pupal
mortality in the Bay Checkerspot butterfly.
Materials and Methods
Large post-diapause larvae were collected in late February and early
March from field sites at Edgewood Park (EW) in 1982 and 1983 and
Morgan Hill (MH) in 1984. Both sites are serpentine grasslands (Krucke-
53
25(l):52-62, 1986
Table 1. Available data on lepidopteran pupal mortality.
Pupal
Major
Species
Mortality
Factor
n
Source
Pieris rapae
.31
parasitoids
large
Harcourt 1966
.38
virus
42
Dempster 1967
.08
virus
27
Dempster 1967
.05
virus
65
Dempster 1967
Papilio machaon
.59
predation
150
Wiklund 1975
.90
predation
158
Wiklund 1975
Papilio xuthus
.83
parasitoids
12
Watanabe 1976
.12
predation
25
Watanabe 1976
Artopoetes pryeri
.45
predation
42
Watanabe & Omata
1978
Papilio glaucus
1.00
predation
112
West & Hazel 1982
.80
predation
109
.88
predation
128
.55
predation
127
Battus philenor
.91
predation
140
West & Hazel 1982
.94
predation
139
.77
predation
80
.96
predation
80
Battus philenor
.14
predation
64
Sims & Shapiro 1983
.67
predation
109
Agraulis vanillae
.08
predation
364
I.L. Brown pers.
comm.
berg, 1984; Sommers, 1984; Crittenden and Grundmann, 1984) where
adverse soil conditions favor the native plants on which the butterflies
depend. Edgewood Park is in San Mateo County at 37° 27' 50" latitude,
122° 17' 10" longitude, and 660' (200m) elevation. Morgan Hill is in Santa
Clara County at 37° 11' 28" latitude, 121° 40' longitude, and 1000' (300m)
elevation. For comparison, Jasper Ridge is in San Mateo County at 37° 25'
latitude, 122° 19' longitude, and 550' (170m) elevation. Rainy weather in
1982 and 1983 and a large population in 1984 (at MH) allowed longer
collection periods than normal. Larvae were kept in groups of about four in
plastic petri dishes (37mm in height, 150mm diameter) and fed daily until
they pupated, on average about a week. They were fed primarily the Eura¬
sian weed Plantago lanceolata L., which they seem to prefer in the
laboratory but which is rarely used in the field (Tilden, 1958). Supplemen¬
tary feeding with the normal foodplants ( Plantago erecta Morris and
Orthocarpus spp.) was done when possible.
As soon as pupae hardened enough to permit handling they were placed
in the field. Transects were laid out in areas from which larvae had been
collected (areas of relatively high larval densities). Pupae were placed
directly on the soil or foliage every 25cm (my span plus 2cm) along the
54
J. Res. Lepid.
transects (Fig. 1). Edgewood Park is open to the public and I wanted my
transects to be inconspicuous to people as well as to potential predators, so
I marked each pupa with a tiny (7 x 4mm) paper flag mounted on an insect
pin. These I could easily relocate. A typed number on the flag identified
each pupa. An acrylic spray (Krylon Crystal Clear 1301) applied to the
page before cutting the flags out made the numbers proof against rain.
Pupae were checked every three to seven days, depending on weather
conditions, and their fates were recorded as follows:
(1) Parasitized — two kinds of parasitoids emerged from pupae. One was
a tachinid fly (Siphost urmia melitaeae Coquillet, determined by Paul
Arnaud, Calif. Academy of Sciences) the larva of which bored out the side
of the pupa and then itself pupated, sometimes near enough to be found.
The exit hole was larger than that made by the piercing predators. The
other parasitoid was a large ichneumonid which caused the pupae to
change to an orangish hue. In emerging from an infected pupa, this wasp
cut a circular cap off the top of the pupa. This cut (Fig. 2) was entirely dif¬
ferent from the typical lines of fracture resulting from butterfly eclosion
(Fig. 3). Butterflies that successfully eclosed left behind a case fractured
along typical lines and very much thinner than that left by even the most
thorough predator.
(2) Stepped on — pupae crushed. The evidence often included signs of
trampling, showing the outline of a footprint, usually of cattle.
(3) Died intact — pupae remaining, apparently unmolested, throughout
the study. They eventually either shrank and were found to be empty, or
they turned black and contained a foul black liquid (probably due to a
virus) .
(4) Vanished — pupae not relocated, although their marking flags were.
None of the traces mentioned below were found.
(5) Predated — pupae clearly damaged by one predator or another. One
predator left behind lA to V2 of the pupal case, the inside of which was well
cleaned out. Another made rough gashes (Fig. 4) and ate most of the con¬
tents, leaving the inside of the case coated with gore. Another predator or
suite of predators pierced the pupal case and sucked out some or all of the
contents. The damage in the two latter cases was consistent with “tasting
but not eating”. Related species are known to be unpalatable as adults and
to a lesser extent as pupae (Bowers, 1980, 1981).
Degree Days (F.) were calculated according to Rahn (1971): [(daily max
<86) + (daily min >50)]/2 -50.
Results
Total pupal mortality ranged from 53 to 89% (Fig. 5). The major mor¬
tality factors, in order of increasing importance, were the following:
Parasitism was a minor factor, taking 1-10% of the pupae. The tachinid
(Siphosturmia melitaeae ) is endemic to virtually all E. editha bayensis
populations, but its average infection rate is only 7.8% (45 samples from
25(1) :52-62, 1986
55
Fig. 2. Remains of E. editha pupa placed in the field at Edgewood Park in 1983.
Note the precise circular break made by a parasitoid as it emerged.
56
J. Res. Lepid.
Fig. 3. Remains of E. editha pupa from which an adult butterfly successfully
emerged. Note the thinness of the cast shell and fracture lines typical of
normal emergence.
1963-1984, 407 tachinids/5212 larvae) and was only 1-2% in these three
samples. Presumably the tachinid infects prediapause larvae, but death of
the host does not occur until the pupal stage. Infected pupae can often be
identified by their low weights. Healthy female pupae average about
380mg and males about 280mg. Tachinid parasitized pupae weigh
under 200mg.
A large ichneumonid was found to oviposit in pupae in the field, a
phenomenon previously undetected. The first observation was actually of
a female (probably parthenogenetic) wasp palping a pupa in the field.
This predatory species is probably generally unimportant, having taken
10/239 pupae in 1982, 3/160 in 1983, and 0/260 at MH in 1984 (nor did it
turn up in a larger sample at MH in 1985) . Since it is necessary to collect or
observe pupae in order to detect it, it is not surprising that this predator is
known to date only from EW.
Crushing generally was found to be a minor factor, but the large number
of cattle grazing at MH raised it to 10% in the 1984 study. There are no cat¬
tle at EW and horses are supposed to be restricted to trails. Cattle were
evicted from Jasper Ridge in 1960 (P. R. Ehrlich pers. comm.).
The proportion of pupae that died intact varied from 9 to 34% and
apparently changed with weather patterns. The higher mortality that
occurred in 1982 was undoubtedly a result of the very unusual cold and
rainy weather. The number of Degree Days measured at Jasper Ridge from
January 1 to March 31 in 1982 was 263, 1983 it was 353, and in 1984 it was
570. 1 expect that this pattern of high mortality occurs whenever late win-
57
25(l):52-62, 1986
ter weather is cold.
Pupae that vanished without a trace before any others in their age class
had eclosed were “taken” by something, presumably a predator. Pupae
disappearing while others in their age class were eclosing might have suc¬
cessfully eclosed and their cast cases might have blown away or been
otherwise removed. This possibility could not be distinguished from
removal by a predator. Here I estimated the proportion of the missing
pupae to have eclosed by taking the proportion of same age class of pupae
which did leave evidence of having eclosed. The remaining proportion I
considered to have been eaten. The effect of this estimate is probably to
underestimate predation (the accuracy of this estimate is important only
in the 1983 sample). Weather-delayed pupae lasted much longer than nor¬
mal in 1983; 42% of them disappeared. In this unusually late year (Fig. 6)
an opportunistic predator (perhaps a bird or rodent) took larger propor-
Fig. 4. Pupa of E. editha placed in the field at Edgewood Park, 1983, showing
evidence of predation. The damage is consistent with “tasting but not
eating” as might occur when a naive predator attacks an unpalatable
subject.
58
J. Res. Lepid.
tions of pupae later in the season. In the other two years this form of mor¬
tality was very low (Fig. 5). This temperature dependent pattern parallels
that observed by Pollard (1979) for Ladoga Camilla (Nymphalidae).
Predators that left physical remains took 23 to 32% of the pupae, making
such predation the least variable factor over the three year study.
One habitat difference at MH allowed a refinement of the experimental
technique used. As at any serpentine grassland site there were small areas
of a fraction to several square meters in which the foliage was extremely
sparse, especially due to lack of the common bunch grasses. These bare
areas at MH alternated with areas of denser foliage so that my transects
regularly passed in and out of them. I recorded whether pupae were placed
in areas of denser foliage, bare areas, or in-between sorts of areas. Analysis
of the data for MH in 1984 showed that pupal mortality varied significant¬
ly with microhabitat (G = 21.41, df = 8, P <.01; Table 2). Being crushed
was more likely in barer spots (G = 8.07, df = 2, P < .025) . Dying intact was
less frequent in barer spots (G = 7.79, df = 2, P <.025). Neither the
“eaten” group nor the “vanished” group varied significantly with micro¬
habitat, but one might add these together as presumed predation. In that
case, predation was less frequent in spots with more foliage (G = 5.992, df
= 2, P = .05). Successful eclosion was not significantly better, but was
nearly so, in spots with more foliage (G = 4.73, df = 2, P <.10).
Table 2. Fates of pupae placed in field at MH in 1984, according to
ground cover of spot where pupae were put.
Bare
Mixed
Dense Foliage
n
Eclosed successfully
.430
.412
.565
122
Died in place
.035
.078
.141
21
Stepped on
.158
.078
.043
26
Eaten
.237
.314
.174
59
Vanished
.140
.118
.076
29
Totals
114
51
92
257
Discussion
The weather of any given study is unusual and this study merely repre¬
sents an extreme of that situation (Kerr, 1985). Both 1982 and 1983 were
very cool, wet, and therefore late years. They differed significantly in that
there were some normally sunny days early in 1982 so that development to
pupation was probably normal. Then the cold set in and pupae became
subject to attack by fungi and viruses. In 1983 there was an extensive
period of cold, but when that ended temperatures were warm enough to
allow normal pupation. On the other hand, 1984, was an extremely dry
year. The rains ended very early and normal temperatures followed. Flight
began and ended early (Fig. 6).
25(l):52-62, 1986
59
Fig. 5. Successful emergence and mortality rates by cause in three samples of
Euphydryas editha pupae which were place in the field.
Fig. 6. Flight seasons of E. editha at Edgewood Park, from first to last adult
seen. Shaded areas represent peak flight.
60
J. Res. Lepid.
Pupation in the field took longer than expected. Laboratory eclosion is
common in 10-11 days and even possible in 7 days, I had expected (in spite
of Tilden’s (1958) estimate of three weeks) normal field times to be about
14 days. In 1983 and 1984 field pupation periods averaged about 18 days
(Table 3) . The average was 27 days in the inclement weather of 1982 and
many pupae (34%) died undisturbed. We have wondered for some ten
years why larvae of Euphydryas editha bayensis do not break diapause
earlier in the winter in order to get through the requisite life stages and
enter diapause before the inevitable spring senescence of their annual
foodplants (Ehrlich et al., 1975). It may be that earlier pupation would too
often lead to longer, often fatal, pupation periods during cooler, rainier
weather of January in the Mediterranean climate of the Bay Area.
The proportion of pupae crushed by cows at MH was great enough to sug¬
gest that this might be an important mortality factor for other life stages of
the butterfly. The animal is probably not significantly exposed to this fac¬
tor when diapausing or when in the adult stage. The observed fifteen day
exposure of pupae resulted in a 10% mortality rate (90% survival rate),
which is equivalent to .993 survival per day. Euphydryas editha probably
spends about 65 days total exposed to crushing as eggs, prediapause and
postdiapause larvae, and as pupae. Therefore I estimate that on the order
of 35% (l-(.993)65) of the total population could be lost to crushing each
generation in colonies where heavy grazing occurs.
Iwasa et al. (1983) have pointed out that pre-emergence patterns of mor¬
tality are critical in analyses of phenomena such as protandry. But the
implications of the data published here (and those collected in Table 1) are
of more general importance. Successful eclosion varied from 11 to 47% of
the pupae placed in the field. Given that estimated adult numbers at Jas¬
per Ridge (H and C) changed from one year to the next year by factors of
0.20 (80% decrease) to 5.00 (400% increase) in Ehrlich’s twenty-five year
study, this four-fold range in pupal mortality makes it clear that mortality
during this stage must be estimated if we are to understand the dynamics
of these populations. Leaving this as a “black box” may make any other
efforts ineffective or inaccurate in explaining observed fluctuations in
numbers.
Table 3. Length of pupation period in the field for Euphydryas editha
bayensis.
Site and Year
n
X
s
95% Cl
Range
EW 1982
47
27.0
7.02
24.9 -29.1
14-43 days
EW 1983
15
17.5
7.01
13.6 -21.4
10-26 days
MH 1984 males
52
19.9
4.38
18.7 -21.1
12-27 days
females
69
16.6
4.04
15.7 -17.6
12.23 days
61
25(l):52-62, 1986
Summary
1. Pupal mortality in the field was high enough in all three years to be a
major factor in determining the sizes of checkerspot butterfly popu¬
lations.
2. The pattern of pupal mortality was variable enough over time to play
an important part in controlling the population dynamics of these
animals; the proportion of pupae successfully eclosing ranged from .11
to .47.
3. Predation by predators leaving remains was the most constant portion
of pupal mortality from year to year.
4. Other mortality factors (predation by predators that left no traces,
being stepped on, and dying intact) varied greatly from one year to the
next.
5. An ichneumonid parasitoid was found which oviposits in and emerges
from pupae of the Bay Checkerspot butterfly.
6. Pupal mortality varies with the amount of foliage around the pupa,
with more foliage resulting in less mortality from predation and crushing,
but more from mold and viruses. More foliage results in a net improve¬
ment in survival rate.
7. Pupation in the field took 18 days under relatively favorable thermal
conditions. Under colder conditions it took as long as 27 days and develop¬
mental failure was common.
Acknowledgments. I gratefully acknowledge my debt to Dennis D. Murphy,
without whose cooperation this work would have been much more onerous. Paul R.
Ehrlich provided access to his group’s accumulated data. Irene L. Brown, Jane L.
Hayes, Dennis Murphy and two anonymous reviewers provided manuscript
critiques.
Literature Cited
BOWERS, M. D., 1980. Unpalatability as a defense strategy of Euphydryas phaeton.
Evolution 34:586-600.
_ , 1981. Unpalatability as a defense strategy of Western checkerspot
butterflies. Evolution 35:367-375.
DEMPSTER, J. P., 1967. The control of Pieris rapae with DDT. I. The natural
mortality of the young stages. J. Applied Ecol. 4:485-500.
_ , 1983. The natural control of populations of butterflies and moths.
Biol. Rev. 58:461-481.
CRITTENDEN, M. & A. GRUNDMANN, 1984. Jasper Ridge. Fremontia 12 (April):20-
21.
EHRLICH, P. R., 1965. The population biology of the butterfly, Euphydryas
editha.U. The structure of the Jasper Ridge colony. Evolution 19:327-336.
EHRLICH, P. R., R. R. WHITE, M. C. SINGER, S. W. McKECHNIE & L. E. GILBERT, 1975.
Checkerspot butterflies: An historical perspective. Science 188:221-228.
EHRLICH, P. R. & COLLEAGUES. Unpublished mark-release-recapture data in
Ehrlich’s Files at Stanford University, Stanford, CA. Collected by Paul and
62
J. Res. Lepid.
his many students 1960-1984.
HARCOURT, D. G., 1966. Major factors in survival of the immature stages of Pieris
rapae (L). Can. Ent. 98:653-662.
IWASA, Y., F. J. ODENDAAL, D. D. MURPHY, P. R. EHRLICH & A. E. LAUNER, 1983.
Emergence patterns in male butterflies: An hypothesis and a test. Theo¬
retical Population Biology 23:363-379.
KERR, R. A., 1985. Wild string of winters confirmed. Science 227:506.
KRUCKEBERG, A. R., 1984a. California’s serpentine. Fremontia 11 (January):ll-
17.
_ , 1984b. The flora of California’s serpentine. Fremontia 12 (April) :3-
10.
POLLARD, E., 1979. Population ecology and change in range of the white admiral
butterfly Ladoga Camilla L. in England. Ecol. Ent. 4:61-74.
RAHN, J. J., 1971. Growing Degree Days of the 1971 growing season. Weekly Weather
and Crop Bulletin March 29, page 11.
SIMS, S. R. & A. M. SHAPIRO, 1983. Pupal color dimorphism in California Battus
philenor (L.) (Papilionidae): Mortality factors and selective advantage. J.
Lepid. Soc. 37:236-243.
SINGER, M. C., 1971. Ecological Studies on the butterfly, Euphydryas editha. Ph.D.
dissertation. Stanford University, Stanford, California.
SOMMERS, S., 1984. Edgewood Park. Fremontia 12 (April): 19-20.
STAMP, N. E., 1984. Interactions of parasitoids and checkerspot caterpillars
Euphydryas spp. J. Res. Lepid. 23:2-18.
STERNITZKY, R. F., 1937. A race of Euphydryas editha Bdv. Can. Entomol. 69:
203-205.
TILDEN, J. W., 1958. Notes on the life history of Euphydryas editha hayensis. The
Lepidopterists’ News 12:33-36.
WATANABE, M., 1976. A preliminary study on population dynamics of the swallow¬
tail butterfly, Papilio xuthus L. in a deforested area. Researches on Popula¬
tion Ecology 17:200-210.
WATANABLE, M. & K. OMATA, 1978. On the mortality factors of the lycaenid butter¬
fly, Artopoetes pryeri M. (Lepidoptera, Lycaenidae). Jap. J. Ecol. 28:367-
370.
WEST, D. A. & W. N. HAZEL, 1982. An experimental test of natural selection for pupa¬
tion site in swallowtail butterflies. Evolution 36:152-159.
WHITE, R. R., 1973. Community relationships of the butterfly, Euphydryas editha.
Ph.D. dissertation, Stanford University, Stanford, California.
WIKLUND, C., 1975. Pupal color polymorphism in Papilio machaon L. and the
survival in the field of cryptic versus non-cryptic pupae. Trans. R. Entomol.
Soc. Lond. 127:73-84.
The Journal of Research on the Lepidoptera
25(l):63-66, 1986
Chromosome Aberrations in the Holocentric
Chromosomes of Philosamia ricini (Saturnidae)
Kunja Bihari Padhy
Department of Zoology, Bonaigarh College, Sundergarh, Orissa, India
Abstract. The nature of chromosome aberrations was studied in Fx male
progeny of irradiated male parents. Translocation rings (0.34%), chains
(3.7%) and fragments (15.9%) were found. Translocation chains outnum¬
bered the frequency of rings and appear to be produced from the latter by
dissociation of chiasma. Dissociation of more than one chiasmata pro¬
duces bivalents and monovalents indistinguishable from the parental
ones. Fragments were transmitted to the Fx offsprings stabily. Inversions
were rare.
Introduction
Chromosome aberrations in the holocentric chromosomes usually
behave in a different pattern from those in monocentrics: fragments are
frequent and are stabily transmitted through several generations (Tempel-
aar, 1979). The nature of observed rearrangements of holocentric
chromosomes in structural hybrids are, however, still doubtful (White,
1973) and to date reports on such aberrations in Lepidoptera are almost
lacking. This perhaps is due to the isodiametric, numerous, much smaller
holocentric chromosomes. In view of the above parameters the present
study was undertaken with Philosamia ricini using 60Co gamma ray source
as the inducing agent.
Methods and Material
Adult males of P. ricini, were irradiated with an acute dose of 60Co
gamma ray (dose rate, 165.5 R/min.). They were held for 24 hours and then
mated to virgin females. The Fx male offspring were examined for meiotic
chromosomal rearrangements. Cytological preparations were stained by
an improved Orcein-Giemsa (OG) technique. Slides were observed and
photographed using high power light microscopy.
Results
Spontaneous chromosome aberrations have been rarely observed in this
species. However, preparations of chromosomes of the Fx male progeny
obtained from the crosses of the irradiated male parent revealed the trans¬
location rings, chains and fragments during the first spermatocytic phase
64
J. Res. Lepid.
(Padhy, 1983). Chromosomal translocations of chains (Fig. 2) and rings
(Fig. 3) included reciprocal exchanges of segments between non-
homologous chromosomes of the irradiated parent. These formed synapses
and chiasmata, usually terminally, characteristic in the Lepidoptera (Fig.
1). Such reciprocal translocations have also been reported in the mite Tet-
ranichus utricae (Tempelaar, 1979). Terminalisation of chiasmata was
also seen in the translocated chromosomes. Terminalization of one of the
chiasmata of a tetravalent ring (Fig. 3) could result in a straight chain of
four (two exchanged) chromosomes with three chiaqsmata intervened
among them (Fig. 2). This structure is frequently noticed (Fig. 4). In the
meiotic spermatocytes bearing the reciprocal translocations of the Fv the
number of bivalents was reduced to 12 (n=14, Fig. 4) or less, excluding the
translocation tetravalent. The translocation chains, however, cannot
result from either fragmentation or differential condensation of chromatin
material because such events were not observed in the gamma irradiated
meiotic preparations of the male parent studied after 12, 24, 48 hour inter¬
vals (Padhy, 1983).
As is clear from Table 1, translocation chains (3.7%) were more frequent
than the translocation rings (0.34%) and are thus about ten times more fre¬
quent. This result indicates a rapid terminalisation of one of the chiasmata
of the tetravalent before metaphase I (Fig. 5A) . Rapid terminalization of
two chiasmata could give rise to two bivalents each attached by a single
chiasma in between (Fig. 5B). These cannot morphologically be differen¬
tiated from normal bivalents and therefore pass undetected. The third
type (Fig. 5C) indicates a chain of three chromosomes attached by two
chiasma which come across in Fx meiosis. The other complement appears
Figs. 1 and 4. Normal diakinesis and metaphase I in spermatocytes.
Fig. 2. Translocation chain in a diakinesis spermatocyte of the F1 male
from the gamma irradiated male parent. Two exchanged and two
nonexchanged chromosomes remain associated by the inter¬
vening chiasmata.
Fig. 3. Metaphase I spermatocyte of the F1 male progeny of the gamma
irradiated male parent. Arrow indicates the translocation quad¬
rivalent with a chromosome complement of 13 bivalents.
25(1) :63-66, 1986
65
b)
o
dj
f 'WWW + /VVAAA'
,+ (VWWV
/WW^ ;
Fig. 5. Mating protocol of the irradiated male P. ricini crossed to a normal
female. F1 male meiosis indicates a translocation ring during diakinesis.
This could possibly give rise to four types of chromosome associations
by thechiasma: a) chains of four, b) chains of two, c) chains of three and
one, and d) four univalents.
+ = chiasma points, / = irradiated, TD = translocation during
diakinesis
Table 1. Frequency of aberrations in the Fx male progeny of the gamma
irradiated male parents of P. ricini.
Stage
Cells
Observed
Translocation
Rings
N
Translocation
Chains
N
Total
Translocations
(%)
Fragments
N
diplotene-
diakinesis
140
2
16
12.8
24
metaphase I
740
1
17
2.4
44
Total
880
3
33
_
68
Control
1000
(0.34%)
(3.7%)
(15.9%)
66 J. Res. Lepid.
as a fragment or univalent. An association of four univalents (Fig. 5D) is
also possible.
The occasional appearance of univalents were noticed in many of the
translocated spermatocytes, but these could not be differentiated from
normal monovalents relative to the dissociation of a single bivalent.
The percentage of translocations was more frequent in late prophase
spermatocytes than in metaphase. The reasons for this are given in Figure
5B which shows that translocations cannot be differentiated morpho¬
logically from the normal complements during metaphase I. This abnor¬
mality in the formation of chiasmata might partly be due to intragenic
alterations and partly due to the absence of a centromere in lepidopteran
chromosomes. The latter explanation is supported by the work of Bauer
(1967) in the Lepidoptera, Murakami and Imai (1974) in Bombyx mori
and Cooper (1972) in the mite Siteropsis graminum.
Fragments were, however, transmitted to the F: structural hybrid in
15.9% of the spermatocytes (Padhy, 1983). Inversions were rare.
Acknowledgments. B. Nayak, Khallikote College, Berhampur, generously
supervised this work.
Literature Cited
BAUER, H., 1967. Die Kinetische Organisation der Lepidopteran-Chromosomen,
Chromosoma, 22:102-125.
COOPER, R. S., 1972. Experimental demonstration of holokinetic chromosomes
and of differential radiosensitivity during oogenesis in the grass mite Siteropsis
gramium (reuter). J. Exptl. Zool. 182:69-72.
MURAKAMI, A. & H. T. IMAI, 1974. Cytological evidence of holocentric chromosomes
of the silkworm Bombyx mori and Bombyx mandarina (Bombycidae, Lepi¬
doptera), Chromosoma, 47:167-178.
PADHY, K. B., 1983. Ph.D. thesis, Utkal University, India.
TEMPELAAR, M. J., 1979. Aberrations of holocentric chromosomes and associated
lethality after X- irradiation of meiotic stages in Tetranichus utricae Koch.
(Acari, Tetranychidae) Mut. Res., 61:259-274.
WHITE, M. J. D., 1973. Animal Cytology and Evolution, 496 pp.
The Journal of Research on the Lepidoptera
25(l):67-70, 1986
Opinion. Opinion is intended to promote communication between
lepidopterists resulting from the content of speculative papers. Com¬
ments, viewpoints and suggestions on any issues of lepidopterology
may be included. Contributions should be as concise as possible and
may include data. Reference should be limited to work basic to the
topic.
Rebuttal to Murphy on Factors to the Distribution of But
terfly Color and Behavior Patterns — Selected Aspects
Benjamin H. Landing
4513 Deanwood Drive, Woodland Hills, California 91364
In reply to Murphy’s critique of my work (Jr. Res. Lep., 1985, 24:4).
Since I think the scientific system ultimately decides the validity of pro¬
positions by scientific criteria, without too much attention to who holds
positions pro or con, and doubt that anyone benefits from further airing of
our differences, however strongly felt, on matters which I don’t think have
much to do with the scientific content of the book, such as why the
material was published in this form rather than some other, whether the
title is misleading, or why the cover is black and white, I am concerned
that the most generally useful response may be none at all. (The butterfly
on the cover, parenthetically, is an Ideopsis juuenta , an oriental region
danaid.) However, since Murphy proposes that he and I have basic dif¬
ferences about various scientific facts and scientific procedures, I will
attempt to make clear my position on several points.
1. Murphy objects to the use of models or general schemes to explain
observations as involving circular reasoning. I disagree, and think this is
exactly the general function of models or general schemes in scientific
reasoning — to bring order to uncoordinated observations or to offer an
explanation of unexplained ones. It is true that making predictions is in
effect proposing explanations for observations not yet made, but this is
normally done in the circumstance that the proposed explanation appears
to explain an observation similar to the one predicted, namely, when that
model has already fulfilled its function. I cannot think of a way of explain¬
ing observations which does not require knowing what at least some
are.
2. I think the definition of ecological niche given by Murphy is inade¬
quate for butterflies because it lacks the qualifier, “. . for each stage of the
life cycle.” I think that a definition which says that adult butterflies and
their caterpillars have exactly the same ecological niches overlooks too
much, and do not see the objection to the concept of niches, or subsets of
68
J. Res. Lepid.
niches, for adult butterflies. The calculations I gave did not specify either
the terms of such niches, nor the number of different possible values of
each term, but simply illustrated what one got if one did make certain
assumptions about these. Murphy and I agree that not all loci contain all
possible niches, which was the point, although (see below) we disagree on
why this is so, at least in part, if the interrelated features of color pattern
and preferred height of flight in the vegetation are part of the definition of
the “niche” of an adult butterfly.
3. Although the book contains a variety of conclusions and propositions
on a variety of matters, I think the single most important part is that
(Chapters 1-5 and parts of others) dealing with the proposed general
scheme, which relates the color patterns of the butterfly species found at a
locus to the height of vegetation at that locus and the preferred height of
flight in the vegetation (from the top down) of butterflies with each
specific category of color patterns. The scheme addresses the fact that, as
one goes north from the tropics in this hemisphere, for example (or up a
mountain in the tropics), specific color patterns disappear in a sequence,
with, as one goes north, transparent patterns dropping out in Mexico,
tiger-stripe (orange with transverse dark stripes) patterns at about the
Texas border, and black with red patterns and black with blue patterns
progressively farther north, so that at about the arctic circle (or above tree
line) the only species truly resident at the locus have as color patterns only
relatively “pure color” white, yellow, orange, blue or lighter brown, or
intergrades of these. Murphy proposes that this is due to the reduction in
total number of species resident at any locus which occurs as one goes
north, but I believe this is not an adequate explanation because it does not
explain the systematic shift in the proportions of species resident at any
locus which have specific color patterns as one does this. The question the
scheme is addressing is not, “why are there fewer transparent or tiger
stripe species in the United States than there are in the tropics?,” for
example, but, “why are there none?”
4. The sequence given above coincides with that given by Papageorgis in
her description of the layering of flight levels of butterflies with various
color patterns in amazonian forests. Murphy says her paper on this is
“controversial,” but not that her description of the layering is incorrect,
and my own field observations in five countries in the American tropics
convince me that it is correct. It is presented as fact (although without
specific attribution) and illustrated by Sbordoni and Forestiero (pages
212-213), for instance.
5. My proposition is that the identity of these two sequences is not an
accident, but reflects the workings of a specific underlying mechanism,
and I supported the proposition that the sequences are what they are
because selection has “geared” color pattern to height of flight in the
vegetation because each pattern is most effectively cryptic at the level in
the vegetation (again, from the top down) at which species with that pat-
25(1) :67-70, 1986
69
tern regularly fly. Murphy says that I did not adequately consider the roles
of “oviposition host selection and breadth, the role of nectar as a limiting
resource, the use of alternative sources of carbohydrates and amino acids,
thermal constraints on butterfly activities, how resources are partitioned,
how butterfly diversity and plant diversity correlate and so on.” I do not
see that any of these necessarily make specific butterfly color patterns
occur or not occur at specific loci, and do not think his list contains the
mechanism. We know for instance, both that closely related species (e.g.,
the viceroy and the red-spotted purple) can develop both color patterns in
different color classes and the appropriately different flight levels, and
that males and females of sexually dimorphic species (e.g., eastern tiger
swallowtail, Diana fritillary) can have patterns in different color classes. I
also do not think that differences in heat-collecting capacity of different
wing colors are the explanation because, for example: 1) the color pattern
group most specifically associated with the deepest part of amazonian
forests is the transparent one, not one of the darker ones, and; 2) the color
patterns persisting in the far north are the lighter “pure color” white,
yellow, orange, blue or brown ones, not the darker ones.
6. I think the next most important section of the book (Chapters 7, 8)
deals with the points that a number of still stated criteria of mimicry sys¬
tems are unnecessary, and in many specific instances not correct. These
include the idea that in Batesian mimicry systems models must be more
abundant than mimics in all loci, and that in Batesian systems models
and mimics, and in Muellerian systems co-models (or co-mimics), must
have the same ranges, because the rules overlooked the point that many
birds migrate. Murphy happens not to criticize this portion of the
book.
7. Murphy sees the data tables as a “smoke screen.” Again, I disagree,
because I do not think one can expect people to evaluate scientific con¬
clusions or propositions without access to the data on which they were
based. Most of the data are not mine originally, as is made clear
throughout, but are derived from the publications of others, and are
assuredly not generally wrong, so I think drawing conclusions from them or
making propositions based on them is not scientifically inappropriate.
The largest data set in the book which is strictly my own is that in the
chapter on interference color patterns, which chapter Murphy happens
not to criticize.
8. The book discusses a variety of other facts which “stick out” of the
data, and offers conclusions or propositions based on them, including:
a) there is, overwhelmingly, a systematic relation between the color
patterns of males and females of sexually dimorphic species, and the
differences follow the pattern of the classes in the general scheme. If the
whole thing is chance, why should this be?
b) the proportions of pierid and lycaenid species which have mistletoe¬
feeding larvae decline disproportionally as one goes north from the
70
J. Res. Lepid.
tropics.
c) toxic/protected papilionids are less likely than Papilio species in the
same regions to show sexual dimorphism with the sexes in different
color classes.
d) toxic/protected species are more likely than others to have similar
color patterns on both upper and lower wing surfaces.
As regards these latter two, since intraspecific Batesian mimicry is
accepted for the monarch, for instance, I don’t think that what amounts to
propositions that intraspecific Muellerian mimicry and, in fact, intra¬
individual Muellerian mimicry, also occur are particularly radical ideas,
but I have never heard either one presented before. To me these again illus¬
trate the importance of access to the data. (A possible volume two,
perhaps unfortunately already over 300 pages long, contains a proposed
explanation of the point on mistletoes, among many other things.)
The Journal of Research on the Lepidoptera
Notes
71
Field Notes on Clossiana improba harryi Ferris (Lepidoptera:
Nymphalidae)
This species was described in 1984 (Ferris, C. D., Bull. Allyn Mus. 89:1-7) from
specimens collected in 1982 by Jack L. Harry of Salt Lake City, Utah. Field collect¬
ing by Ferris in 1984 and in 1985 by Lisa Snyder from the Audubon Ecology Camp
of the West (University of Wyoming Trail Lake Ranch), near Dubois, Wyoming,
has increased our knowledge of this species with respect to its behavior and
geographic distribution.
This butterfly is a denizen of remote, high-alpine areas (above 11,000' (3355 m))
as shown in the type locality photograph (Fig. 1). It flies in early August, and was
known originally only from the vicinity of Mt. Chauvenet in the Wind River Range
of central -western Wyoming in Fremont Co. The type locality is situated in the
Popo Agie Primitive Area of the Shoshone National Forest. C. i. harryi was des¬
cribed originally as occurring in eleven colonies extending for approximately 4.5
miles along the Bears Ears Trail. In 1984, I found that the distribution in this
region is not discrete, but rather continuous from west of Adams Pass to west of Mt.
Chauvenet. In 1985, Snyder discovered two additional colonies of harryi in the
Fitzpatrick Wilderness Area at Goat Flat and Ram Flat. These localities are re¬
spectively 40 and 45 air miles NW of the type locality, also in the Shoshone
National Forest in Fremont Co. Figure 2 is a map of this butterfly’s range, as
currently known.
The habitat of this species is in relatively level, somewhat xeric, areas of granitic
Fig. 1. Type locality (looking to the West) and typical habitat of C. improba
harryi.
72
J. Res. Lepid.
Fig. 2. Map showing the distribution (cross-hatched circles) of C. improba
harryi. Only the larger lakes are shown. The dotted lines are hiking
trails.
gravel on which mats of the larval hostplant ( Salix arctica Pall) grow abundantly.
This plant is widespread throughout alpine areas of Wyoming, but the butterfly is
very local. Adults of harryi dorsally bask on gravel patches and on the pale granite
boulders distributed over their habitat. From the rather dark aspect of museum
specimens of this species, one would think that these butterflies would be very con¬
spicuous against the pale background of the gravel and boulders. This is not the
case, however, in the field. The pale central areas of the wings (dorsally) produce a
cryptic pattern which blends very well with rocky substrates and renders the but¬
terflies difficult to detect.
To date, this species has been found only on the east slope of the Wind River
Range in Fremont Co., Wyoming. The eastern slope of the Range is considerably
drier than the western slope which supports many butterfly fauna. It will be sur¬
prising if harryi is not eventually discovered in neighboring Sublette Co., at
appropriate elevation, on the western slope of the Wind River Range. Access to
suitable habitat areas, however, is only by foot or horseback over 20 miles or more of
rugged terrain. This butterfly is abundant once a colony has been located, and is in
no sense endangered, as may possibly be the case for its sibling species in Colorado
C. acrocnema (Gall & Sperling).
Clifford D. Ferris, P. 0. Box 3351, University Station, Laramie, Wyoming 82071 -
3351
INSTRUCTIONS TO AUTHORS
Manuscript Format: Two copies must be submitted (xeroxed or carbon papered),
double-spaced, typed, on 8V2 x 11 inch paper with wide margins. Number all pages
consecutively and put author’s name at top right corner of each page. If your typewriter
does not have italic type, underline all words where italics are intended. Footnotes,
although discouraged, must be typed on a separate sheet. Do not hyphenate words at the
right margin. All measurements must be metric, with the exception of altitudes and
distances which should include metric equivalents in parenthesis. Time must be cited on
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be cited as example: 4. IV. 1979 (day-arabic numberal; month-Roman numeral; year-
arabic numeral). Numerals must be used before measurements (5mm) or otherwise up to
number ten e.g. (nine butterflies, 12 moths).
Title Page: All papers must have the title , author’s name, author’s address, and any
titular reference and institutional approval reference, all on a separate title page. A
family citation must be given in parenthesis (Lepidoptera: Hesperiidae) for referencing.
Abstracts and Short Papers: All papers exceeding two typed pages must be ac¬
companied by an abstract of no more than 300 words. An additional summary is not
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include the full scientific name with author (not abbreviated) andyear of description. New
descriptions should conform to the format: male: female, type data, diagnosis, distribu¬
tion, discussion. There must be conformity to the current International Code of
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References: All citations in the text must be alphabetically listed under Literature Cited
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Tables: Tables should be minimized. Where used, they should be formulated to a size
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Number legends consecutively with separate paragraph for each page of illustrations. Do
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comments of reviewers.
THE JOURNAL OF RESEARCH
ON THE LEPIDOPTERA
Volume 25 Number 1 Spring 1986
IN THIS ISSUE
Date of Publication: October 1, 1986
Hidden Genetic Variation in Agraulis vanillae incarnata
(Nymphalidae)
Thomas E. Dimock & Rudolf H. T. Mattoni 1
Electrophoretic Evidence for Speciation within the Nominal
Species Anthocharis sara Lucas (Pieridae)
Hansjurg Geiger & Arthur M. Shapiro 15
Genetic Differentiation Between Subspecies of Euphydryas
phaeton (Nymphalidae: Nymphalinae)
A. Thomas Vawter & Janet Wright 25
On the Monophyly of the Macrolepidoptera, Including a
Reassessment of their Relationship to Cossoidea and Castnioidea,
and a Reassignment of Mimallonidae to Pyraloidea
James A. Scott 30
Electrophoretic Confirmation of the Species Status of Pontia
protodice and P. occidentalis (Pieridae)
Arthur M. Shapiro & Hansjurg Geiger 39
Susceptibility of Eggs and First-Instar Larvae of Callosamia
promethea and Antheraea polyphemus to Malathion
Thomas A. Miller, William J. Cooper & Jerry W. Highfill 48
Pupal Mortality in the Bay Checkerspot Butterfly (Lepidoptera:
Nymphaqlidae)
Raymond R. White 52
Chromosome Aberrations in the Holocentric Chromosomes of
Philosamia ricini (Saturnidae)
Kunja Bihari Padhy 63
Opinion: Rebuttal to Murphy on Factors to the Distribution of
Butterfly Color and Behavior Patterns — Selected Aspects
Benj amine H. Landing 67
Notes 71
COVER ILLUSTRATION: Selectively bred adults of Agraulis vanillae incarnata, see
Dimock and Mattoni, pages 1-14.
THE JOURNAL
OF RESEARCH
ON THE LEPIDOPTERA
K
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SD
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x§
THE JOURNAL OF RESEARCH
ON THE LEPIDOPTERA
The Lepidoptera Research Foundation, Inc.
c/o Santa Barbara Museum of Natural History
2559 Puesta Del Sol Road
Santa Barbara, California 93105
William Hovanitz
Rudolf H. T. Mattoni, Editor
Lorraine L. Rothman, Managing Editor
Scott E. Miller, Assistant Editor
Emilio Balletto, Italy
Miguel R. Gomez Bustillo, Spain')'
Henri Descimon, France
Thomas Emmel, U.S.A.
Lawrence Gall, U.S.A.
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Hansjuerg Geiger, Switzerland
Otakar Kudrna, Germany
Dennis Murphy, U.S.A.
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Arthur Shapiro, U.S.A.
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'('Deceased December 17, 1985
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Treasurer is Barbara Jean Hovanitz. The Board of Directors is comprised of Barbara Jean Hovanitz, Lorraine
L. Rothman, and R. H. T. Mattoni. There are no bond holders, mortgages, or other security holders.
ISSN 0022 4324
Published By:
Founder:
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Associate Editors:
Journal of Research on the Lepidoptera
25(2): 73-82, 1986(87)
A New Species of Calisto from Hispaniola with a Review
of the Female Genitalia of Hispaniolan Congeners
(Satyridae)
by
Kurt Johnson
Department of Entomology, American Museum of Natural History, Central Park West
at 79th St., New York, New York 10024,
Eric L. Quinter
37-06 72nd Street, Jackson Heights, New York 11376
and
David Matusik
Department of Entomology, Field Museum of Natural History, Roosevelt Road, Chicago,
Illinois, 60605
Abstract. Calisto ainigma , new species, is described from a unique
holotype female collected at Jarabacoa, Dominican Republic in 1985.
Female genitalia, not previously studied in Calisto , are compared for
twenty-two Hispaniolan congeners. Of all congeners, wing patterning
in C. ainigma only slightly resembles C. elelea Bates, a species of
limited Haitian distribution. Female genitalia suggest the two may be
distant sister species.
Introduction
The diversity of the satyrid genus Calisto is remarkable. With the
recent work of Schwartz (1983a, 1983b, 1987 [in press]) Schwartz and
Gali (1984) and Gali (1985), twenty-five Calisto species are recognized
as occurring on Hispaniola. Eleven of these result from work of
Schwartz and Gali in seldom collected areas of Hispaniola and repre¬
sent endemic taxa with extremely limited known geographic ranges.
This latter characteristic of Calisto led Schwartz and Gali (1984, p. 10)
to suggest the discovery of further endemic Calisto from Hispaniola as
inevitable. Genericly, Calisto are endemic to the Antilles and characte¬
rized by each of the islands exhibiting various endemic species (Mun-
roe, 1950). Given the increasing diverity of Calisto taxa recognized as
occurring on Hispaniola (11: Bates, 1935, 1939; 12: Michener, 1943; 14:
Clench, 1943a, 1943b; Riley, 1975; 20: Schwartz and Gali [see p. 1]; 25:
Gali, 1985) it may be anticipated that when adequately sampled, Cuba
may also yield a diversity of Calisto taxa. With the appearance of
74
J. Res. Lepid.
Schwartz’s (1983a; 1987 [in press]) treatments of Hispaniola butter¬
flies, an ample amount of data concerning the taxonomy and distribu¬
tions of Hispaniolan Calisto has now been accumulated.
Characteristic of the results of Schwartz and Gali’s work has been
documentation that among the few cosmopolitan Hispaniolan Calisto
(like confusa Lathy and obscura Michener) there occurs a number of
other endemic species characterized by (a), marked wing pattern differ¬
ences from the previously known congeners and slight, if any, sexual
dimorphism and (b). extremely limited local known distributions often
marked by restriction to a single known locality or limited habitat. The
former results from the lack of comprehensive collecting prior to the
work of Schwartz and Gali; the latter reflects the often extreme
fragmentation of the native habitats of the island, remnants of which
are now often only found in very limited undisturbed areas of inaccessi¬
ble topography. This latter factor also seems to explain the lack of any
recent association of specimens with the names C. montana and C.
micheneri Clench (1943a, b). The holotypes of these species have been
illustrated by Riley (1975) but both are from localized and remote
localities from which no further specimens have been taken in recent
years.
Hitherto, all studies of Calisto have examined characters solely of the
wing and male genitalia. Given the recent accumulation of studies of
Calisto cited above, an examination of female genitalia of the group is
requisite and timely. Further, such an examination has been required
by the collection in the Central Cordillera in 1985 of a female specimen
of Calisto (hereinafter in introduction referred to as “the Jarabacoa
female”) with wing pattern quite unlike any previously known taxon of
the genus (Albert Schwartz, pers. comm). Matusik captured the speci¬
men while he and Johnson were collecting along a stream near Jaraba¬
coa, La Vega Province, Dominican Republic, June 26, 1985. A perfectly
fresh specimen, it had attracted attention because amongst extremely
common C. obscura and C. confusa which “flash” brown and submar¬
ginal white when flying, this specimen was markedly yellowish. Upon
capture, the several unique traits noted in the following diagnosis were
obvious and further heightened interest in the specimen. Unfortunate¬
ly, due to pre-arranged itinerary the collectors had to leave the area
that day; they returned with additional local collectors a week later but
concerted Calisto collecting yielded no further examples.
Fig. 1. Female genitalia of Flispaniolan Calisto. Format, each entry, above:
papillae anales, lateral view; below: genital plate, ductus bursae and corpus
bursae, ventral view. A. C. elelea (AMNH), Sierra de Baoruco, 12 km. from
Las Abejas on Las Abejas highway, Dominican Republic [D. R.], 400 m.,
May, 1984, D. Matusik; B. C. ainigma, holotype (AMNH); C. C. obscura,
paratype (AMNFI), Puerta Plata, D. R., 7-8 May 1915; D. C. confusa (AMNH),
Trujillo City, D. R., 1946, A. L. Stillman; E. C. debarriera (AMNH), 10 km. SE
Constanza, D. R., 1270 m., D. Matusik; F. C. batesi, same data as A.; G. C.
lyceia Bates (MCZ), Isla Saone, D. R.; H. C. tragia (ASC), 1-4 km. WNW
25(2): 73-82, 1986(87)
75
Fig. 1. (Cont). Scierie, Sud-Est, Haiti [H], 2000 m., 4 September 1984,
A. Schwartz; I. C. micrommata (ASC), 2 km. NE Puesto Piramide 204, La
Estrelleta, D. R., 1700 m., 16 July 1983, A. Schwartz; J. C. sommeri (AMNH),
38 km. marker, 2 km right turn to Nursery, highway to Las Abejas, D. R.,
1600 m., May, 1984, D. Matusik; K. C. hysia Godart (AMN), Paradis, D. R.,
600 m., 15 August 1932; L. C. grannus (ASC), 21 km. SE Constanza, La Vega,
D. R., 2500 m., 10 July 1980, A. Schwartz.
76
J. Res. Lepid.
The Jarabacoa female was donated to the AMNH and has since been
studied in more detail, along with examination of the relevant litera¬
ture, specimens from the collections of the junior author, AMNH, Allyn
Museum of Entomology, Museum of Comparative Zoology (Harvard)
(MCZ), Albert Schwartz (ASC) and Frank Gali, and female genitalia of
Hispaniolan congeners represented in these collections (Figs. 1 and 2).
There has been considerable discussion amongst students of Hispa¬
niolan butterflies concerning the status of the Jarabacoa female con¬
sidering its extremely unique wing markings and occurrence at one of
the most frequently collected localities on Hispaniola. Schwartz (pers.
comm.) advised that even though its markings did not seem closely
comparable with any known Calisto, the specimen must be suspected
as a possible aberration of either of the common local congeners,
C. confusa or C. obscura. Dissection of the unique Jarabacoa female
has revealed a genitalic configuration differing radically from both
C. confusa (Fig. 1, D) and C. obscura (Fig. 1, C) as represented by
topotypical, paratypical and syntopic/synchronic examples. In addition,
the genitalia of the Jarabacoa female do resemble those of another
known Calisto (Fig. 1, A) and further examination of this latter taxon
has indicated certain wing pattern similarities (Fig. 3). As a result,
these data suggested three alternative treatments concerning the
Jarabacoa female:
1. Conclude from the wing pattern and genitalic characteristics that
it represents an undescribed species of Calisto whose taxonomic posi¬
tion in the genus is concordant ( sensu Murphy and Ehrlich, 1984, p. 27)
with an overall view of morphological and biogeographic characteristics
of the group.
2. Conclude by speculation that it is an aberration of some previously
described species of Calisto , though the latter cannot be designated
because of the divergent wing morph of the former.
3. Accord no published recognition to the unique specimen pending
further sampling.
We believe that genitalic and wing character evidence assembled in
this study (Figs. 1—3) along with the highly insular nature of many
Calisto distributions warrants the first kind of treatment. We would
have accepted the second treatment if the genitalia of the Jarabacoa
female had resembled any geographically proximate congener. We
Fig. 2. Female genitalia of Flispaniola Calisto, continued. Format as in Fig.
1. A. C. areas (ASC), 14 km. SE Constanza, La Vega, D. R., 2100 m., 20 July
1985, A. Schwartz (small letters referenced in text); B. C. crypta Gali (AMNH),
Monte Christi, D. R., 13 March 1931, A. L. Stillman; C. C. franciscoi (ASC),
8 km. ESE Canoa, Barahona, D. R., 28 July 1985, A. Schwarts; D. C. hender-
soni (ASC), 4 km. E El Limon, Independencia, D. R., 2 April 1984, A. Sch¬
wartz; E. C. schwa rtzi (AMNH), same data as Fig. 1, J; F. C. clydoniata
(ASC), 2 km. NE Puesto Piramid 204, La Estrelleta, D. R., 1400 m., 13 August
1983, A. Schwartz; G. C. galii (ASC), 10 km. SE Constanza, D. R., 1800 m.,
25(2): 73-82, 1986(87)
77
Fig. 2. (Cont). 9 July 1980, A. Schwartz; H. C. clenchi Schwartz and Gali
(ASC), 5 km, Ne Los Arroyos, Pedernales, D. R., 1800 m., 30 June 1983, A.
Schwartz; I. C. chrysaoros Bates (ASC), 5 km. NE Los Arroyos, Pedernales,
D. R., 1800 m., 4 October 1983, A. Schwartz; J. C. neiba Schwartz & Gali
(ASC), 15 km. S. Elias Pina, La Estrelleta, D. R., 1100 m., 26 July 1981, A.
Schwartz.
78
J. Res. Lepid.
Fig. 3 Eight under surface similarities between C. ainigma (left) and C.
elelea (right). 1. completely red-orange discal cell; 2. lightened apical
ground color; 3. outline of marginal band ( elelea ) (fully black in
ainigma ); 4. light post-basal line; 5. darkening costad in medial area;
6. darkening costad in limbal area; 7. light mesial line extending from
anal angle basad hindwing ocellus; 8. darkened spot at anal angle.
consider the third action inappropriate because (a), there has been a
paucity of study of female genitalia in Calisto hitherto (see Remarks),
(b). lack of such study has left a number of variant females cited in the
literature as undetermined and (c). not recognizing the wing and
genitalic features of the Jarabacoa female would result in loss of their
potential taxonomic and biogeographic information as regards ongoing
studies of Calisto. We therefore propose the following:
Calisto ainigma, Johnson, Quinter & Matusik, new species
Figs IB, 3A, 4
Diagnosis. Distinguishable from all other known Calisto by the following
marked characters: (1). undersurface ground color distinctly yellow to ochre
[yellower than in photo (Fig. 4), such hues caused by differential spacing of
deep brown scales amongst bright yellow scales], not brown or grey as on
congeners; (2). both wing undersurfaces with wide (1 mm.) olive-black margin¬
al band, not occurring on any congener; (3). aside from unique marginal band,
hindwing lacking any bands (congeners variously have postbasal medial,
postmedial and/or submarginal bands of various colors and/or a dark basal disc
with its distad margin bandlike [C. montana, C. micheneri ]). Rather, C.
25(2): 73-82, 1986(87)
79
ainigma has a yellow ground color appearing as blackish-grizzled from the
wing base distad to an indistinct medial juncture with purer yellowish ground
color distad in the postmedian areas to margin. Intense blackish-grizzling
centered costad along this medial juncture, along with invasion basad of the
marginal line in cells Mi and M2, adds further oddity to the pattern; latter
suffusions resemble C. elelea Bates (Fig. 3) which is otherwise banded; (4). as
only in C. montana, C. micheneri, and C. tragia Bates, hindwing with single
ocellus [cell CUi] devoid of any obvious surrounding patterning [not with [a],
single ocellus surrounded by various maculation expansive distad (C. confusa,
C. obscura, C. hysia Bates, C. elelea, C. clydoniata Schwartz and Gali) or [b].
two ocelli, one at each end of the limbal area (C. grannus Bates, C.
micrommata Schwartz and Gali, and C. sommeri Schwartz and Gali)]; C.
ainigma, like C. elelea, has distinctly lighter ground color based cell CUx
ocellus, in latter a band; (5). hindwing undersurface with two white dots in
cells M2 and M3 (not with three in cells M2 to Rs as in C. galii Schwartz [see
Remarks for further significance of this feature].
Description. Male. Unknown. Female. Uppersurface of the Wings: Ground
color ochre-tinted olive brown, especially distad, with wings darker olive basad.
Otherwise no distinctive markings. Undersurface of the Wings: Forewing
ground color ochre- tinted olive with prominent subapical ocellus [diameter 2.8
mm.], black centrad, ringed yellow and with two blue-white dots within.
Surrounding subapical area and adjacent postmedian area sheened lighter
yellowish olive. Prominent 1 mm. olive black marginal band. Hindwing ground
color yellowish-ochre; except for 1 mm. wide olive-black marginal band, with¬
out any other bands. Rather, blackish-grizzling proceeds from wing base to
variously distinct medial juncture with yellow-ochre ground color distad on
remainder of wing. Blackish grizzling concentrates costad along this medial
juncture; marginal band intrudes basad in cells M2 and Mi. Distad medial
juncture of black grizzling, yellowish ground color broken only by two white
dots in cells M2 and M3 and small but prominent ocellus [diameter 1.0 mm.] in
cell CU2, black centrad, ringed yellow and with white dot within. Forewing
length: 16 mm. Male Genitalia. Unknown. Female Genitalia. Fig. IB. Of
congeners studied, sharing with C. elelea (a), thickened ring of genital plate
(see Remarks), ring heavily “wrapped” with membranous folds obscuring
widened under-lying sclerotized ring which in other ringed taxa (see Remarks)
is thinner and not heavily membranous, and (b). dorsad configuration of the
ring comprised of two bilaterally symmetrical widened areas, extremely thick¬
ened and bulbous relative to congeners and which on C. ainigma shows a
tapered, dorsad pointing extension. Corpus bursae markedly shorter on C.
ainigma than C. elelea and with signa of former located far cephalad the
juncture of this bursae with the membranous ductus bursae.
Type. Holotype, female, deposited AMNH, La Vega Province, Dominican
Republic, 930 m. in central portion of Cordillera Central, June 26, 1985, by
David Matusik at site characterized as follows: along a small (1.5— 2.5 m. wide)
stream currently running between the Hotel Pinar Dorado’s group of “caba¬
nas” and the highway that proceeds from the immediate entrance to the hotel
grounds about 4 km. northwest to central Jarabacoa (which is expanding its
outer perimeter by active outlying home development). Stream crosses a fenced
cattle grazing break between the stands of Australian Pine which border it
west along the highway and east east of the cabanas. Specimen taken in grass
80
J. Res. Lepid.
along this stream about 300 meters north of the hotel and its entrance to the
highway (e.g. ca. 4 km. southeast of Jarabacoa).
Remarks. Schwartz (1983a, fig. I, J) and Schwartz and Gali (1984) mention
variant females which they either associate as aberrants with known Calisto
taxa or which show facies leading them to conclude “another species of Calisto
presumably occurs in the Cordillera Central” (Schwartz and Gali, 1984, p. 10).
Concerning these, and undescribed taxa currently being described by Schwartz
or Schwartz and his colleagues, Schwartz (pers. comm.) has assured us that
none is similar enough to the facies of C. ainigma to warrant discussion here.
The genitalic survey conducted during this study warrants the following
general remarks.
Characters of the female genitalia apparently provide a far more useful
reference for Calisto than those of males. Male genitalia of Calisto , which have
been reviewed to some extent by nearly all authors cited herein, are mostly
alike. Minor but consistent differences have been cited, particularly by Michen-
er and Schwartz et al., to distinguish various taxa which also have distinctive
wing pattern characters. Within Calisto, as presently defined, the only radical¬
ly divergent male genitalia amongst Hispaniolan taxa occur in C. elelea, C.
pulchella Lathy, C. areas and C. raburni Gali. As can be seen in Figs. 1 and 2,
such divergence is reflected in the female genitalia of both C. elelea and C.
areas, though the former is more like other Calisto. C. pulchella is not figured
becaused its female genitalia are so divergent as to suggest lack of recognizable
homology with other taxa presently placed Calisto, a matter presently under
study. C. raburni is recently described and its female unknown.
Two general genital plate configurations are apparent in Calisto studied,
those with two obvious components and those with only one. Other taxa are
intermediate between these extremes. C. areas (Fig. 2A) best exemplifies a two
component structure: a sclerotized ring (Fig. 2A, a) with a sculptured dorsal
crown (Fig. 2A, b) and a sclerotized ductal tube (Fig. 2A, c) with dorsad “horns”
(Fig. 2A, d). In C. franciscoi Gali and C. hendersoni Gali (Fig. 2C, D) apparent
remants of these horns appear within a configuration otherwise characterized
by distinct separation of the ring and crown. C. schwartzi Gali (Fig. 2E) exhibits
remants of the horns closely allied with the ring and crown combination. In the
remaining Calisto (Fig. 1, 2F, F-J) the ring, closely combined with the crown,
forms a generalized configuration. However, within this group some taxa
exhibit a sclerotized loop within the ring (Fig. 1C, F-L), or without a loop,
variously developed cephalad pointing prongs (Fig. 1, A, B, D-J). The particu¬
lar structure characterizing C. elelea and C. ainigma has been described in the
above description. Within Calisto there are also apparent differences in the
configurations of the papillae anales, ductus bursae and corpus bursae with its
associated signa. It is likely that these characters will prove very useful in
examining the taxonomic and biogeographic relations of the Calisto endemic to
various Antillean islands. Such a study is in progress. At present it is important
to note that female genitalic characters corroborate the species statuses
accorded the numerous presently recognized species in Hispaniola, and particu¬
larly of interest those named very recently by Schwartz and Schwartz and Gali
[see p. 1]. The only exception might be C. confusa and C. debarriera Clench
which , though considered full species on biological grounds (Schwartz, pers.
comm.) are very similar compared to other congeners. As regards the often
25(2): 73-82, 1986(87)
81
debated species status of C. hysius ssp. batesi Michener (Clench, 1943b;
Schwartz, 1983a; Riley, 1975), female genitalia appear to provide a moderately
strong argument supporting C. batesi’ s specificity.
The similarity in female genitalic facies of C. ainigma and C. elelea was
unanticipated. The latter species has a highly insular distribution limited to
montane areas surrounding Port-au-Prince, Haiti. Subsequently noted similar-
Fig. 4. Holotype female, Calisto ainigma , new species. Left, upper surface
of the wings; Right, under surface of the wings.
ities in certain aspects of the wings patterns of C. elelea and C. ainigma (Fig. 3)
are likewise suggestive and have invited the conclusion that the facies of C.
ainigma is not so extraordinary as originally presumed by us and other
workers familiar with Hispaniolan Calisto (e.g. Schwartz, pers. comm.). Male
genitalia of C. elelea are distinctive such that among Calisto Brown and
Heineman (1972, based on Michener, 1943) placed this species within a
monotypic species group. It will be of extreme interest whether the male of
C. ainigma, once discovered, further corroborates C. ainigma’s placement
with C. elelea as a sister taxon.
Etymology. The name is Greek for “enigma”, referring to the curious wing
pattern, occurrence at the often collected Jarabocoa area, and unanticipated
suggested sister species relationship to C. elelea. Upon the suggestion of
Schwartz and Gali (1984) and Gali (1985) species names in this paper have
been made to conform to the feminine gender of the name Calisto. A single
exception is C. grannus, the origin of which name Schwartz states is indeter¬
minate.
Acknowledgements Albert Schwartz (Miami Dade County Community Col¬
lege, Miami, Florida) kindly reviewed drafts of the manuscript and supplied
various female Calisto for dissection. Lee D. Miller (Allyn Museum of Entomol¬
ogy of the Florida State Museum, Sarasota, Florida) and Frederick H. Rindge
(AMNH) also reviewed the manuscript. Luis Marion (Santo Domingo, Domini¬
can Republic) and Robert R. Postelnek (Skokie, Illinois) kindly facilitated
aspects of this work.
82
J. Res. Lepid.
Literature Cited
BATES, M. 1935. The satyrid genus Calisto. Occ. Papers Boston Soc. Nat. Hist. 8:
229-248.
BROWN, F. M. & B. HEINEMAN. 1972. Jamaica and its Butterflies. E. W. Classey,
Ltd., London, sv + 478 pp.
CLENCH, H. K. 1943a. Some new Calisto from Hispaniola and Cuba (Lepidoptera:
Saryridae). Psyche 50: 23-29.
CLENCH, H. K. 1943b. Supplementary notes on Calisto (Lepidoptera: Satyridae).
Psyche 50, unnumbered page.
GALI, F. 1985. Five new species of Calisto (Lepidoptera: Satyridae) from Hispa¬
niola. Milwaukee Public Museum Cont. to Biol, and Geol. 63: 16 pp.
MICHENER, C. D. 1943. A review of the genus Calisto. Am. Mus. Novt. 1236: 1-6.
MUNROE, E. G. 1950. The systematics of Calisto. (Lepidoptera, Satyrinae), with
remarks on evolutionary and zoogeographic significance of the genus. J.
New York Ent. Soc. 58: 211-240.
MURPHY, D. D. & P. R. EHRLICH. 1984. On butterfly taxonomy. J. Res. Lepid. 23:
19-34.
RILEY, N. D. 1975. A Field Guide to the Butterflies of the West Indies. New York
Times Book Co., New York, 224 p.
SCHWARTZ, A. 1983a. A new Hispaniolan Calisto (Satyridae). Bull. Allyn Mus.
80: 1-10.
SCHWARTZ, A. 1983b. Haitian Butterflies. Mus. Nac. Hist. Nat., Santo Domingo,
69 p.
SCHWARTZ, A. 1987, in press. The Butterflies of Hispaniola. Mus. Nac. Hist. Nat.,
Santo Domingo.
Journal of Research on the Lepidoptera
25(2): 83-109, 1986(87)
Records of Prolonged Diapause in Lepidoptera
Jerry A. Powell
Department of Entomological Sciences, University of California, Berkeley
Abstract. Previously unpublished records of diapause and adult em¬
ergence one or more years beyond that of other individuals in the
species are reported for 19 species of moths in 8 superfamilies. Records
of prolonged diapause are summarized, representing 90 species in 10
superfamilies. Prodoxidae, Saturniidae, Pieridae, and Papilionidae
predominate, but other taxa may be disproportionately underrepre¬
sented owing to lack of study. In Lepidoptera, extended diapause
occurs in prepupal larvae or pupae and is most often observed in
species that live in areas of seasonal drought and in cone- and
seed-feeding species that depend upon crops of erratic abundance. We
do not have convincing evidence for a genetically fixed polyphenic
expression, wherein a small number of individuals carryover irrespec¬
tive of environmental conditions.
Prolonged diapause is the maintenance of the dormant state in insects
for one or more years beyond the period of emergence by most
individuals in the population. There have been many records of
the phenomenon in Lepidoptera, particularly in butterflies and
Saturniidae, most often originating from pupae held indoors or in
climates distant from the natural ones. In the past such records were
regarded as aberrant, even astonishing occurrences that had no
particular biological significance. Few researchers were sufficiently
interested to carry out controlled experimental research on the
relationships between the underlying genetic variability and en¬
vironmental factors that might demonstrate causes and possible
adaptive values of prolonged diapause.
In recent years, however, a number of reports suggest that in many
insects multiannual delay of development is neither anomalous nor
even exceptional and that it may have important adaptive significance
(e.g., Danks, 1983; Hedlin et al., 1982; Nakamura & Ae, 1977; Shapiro,
1981; Sunose, 1978; Takahashi, 1977; Tauber et al., 1986). A selective
advantage of facultative carryover seems to be especially true in cone-
and seed-feeding species that depend upon hosts that produce seed
crops of erratic abundance (e.g. Hedlin, 1967; Hedlin et al., 1982;
Nesin, 1984; Sunose, 1978) and in desert insects, both phytophagous
and predaceous (e.g. Ferris, 1919; Comstock & Dammers, 1939; Linsley
& MacSwain, 1945, 1946; Nakamura & Ae, 1977; Powell, 1974, 1975,
1984b, present data).
84
J. Res. Lepid.
Twelve years ago I summarized some examples of prolonged diapause
in various insects (Powell, 1974), and that paper has been cited several
times as though it was a review of the subject, but it is not. Recently
two more comprehensive reviews have appeared (Sunose, 1983; Usha-
tinskaya, 1984). Sunose reviewed my records as well as others and
tabulated 64 insect species in which the dormancy has been reported to
extend more than a year. Ushatinskaya, evidently unaware of the
Sunose compilation, listed a similar number, many of which had not
been noted by Sunose. These include eggs of grasshoppers, first instar
larvae of parasitic Hymenopera and of tachinid flies that live within
sawfly or moth larvae which undergo prolonged diapause, first or last
instar larvae of gall gnats, mature larvae of bees, sawflies and meloid
beetles, and adults of chrysomelid beetles. In Lepidoptera multiannual
dormancy is known only in prepupal larvae or pupae, although in many
species diapause occurs in eggs, first or second instar larvae, or adults.
Sunose (1983) listed records of prolonged diapause in 20 species of
Lepidoptera, and Ushatinskaya (1984) tabulated 14, of which 10 are
additions to Sunose’s total. There are a great many more instances
known. Probably any lepidopterist who has reared many Papilionidae
or Saturniidae is familiar with carryover pupae and emergences of the
adults in later years. I have assembled a list of records representing
about 90 species, including those reported here (Table 1). These have
been reported in more than 60 bibliographic references and several
unpublished personal communications. Even excluding the yucca
moths (Prodoxidae), which are restricted to North America and for
which I have scores of delayed dormancy rearings, about 65% of the
records are for Nearctic species. This implies that search of Old World
literature has been cursory, and that the phenomenon is known in
many more species than I have compiled. In fact, it would be impossible
to collect a complete list of references to prolonged diapause because
often its records are buried in life history studies, reports on insects of
economic concern, or in taxonomic works.
My purposes here are to record previously unpublished instances of
delayed emergence in a diversity of moth taxa and to call attention to
the likelihood that prolonged diapause is much more prevalent in
Lepidoptera than previously supposed. For example, four of the occurr¬
ences listed below are species of Pyralidae, Geometridae and Noc-
tuidae. These are families for which I have done only incidental
rearing, and therefore one might expect records of extended dormancy
to be commonplace in these taxa, yet I have seen few published. This
suggests that diapause may be prolonged commonly in these large
families, but students have not had sufficient patience to continue
surveillance of pupae that do not develop in the first season and to test
them in various artificial overwintering regimes. Diapause develop¬
ment is a dynamic process that takes place over weeks or months in
North Temperate Zone insects, and the physiological responses to
25(2): 83-109, 1986(87)
85
Table 1. Taxonomic and geographical distribution of some Lepidoptera in
which prolonged diapause is recorded
MONOTRYSIA
Prodoxidae
DITRYSIA
Tineidae
Coleophoridae
Gelechiidae
Ethmiidae
Tortricidae
(Olethreutinae)
Cochylidae
Pyralidae
Geometridae
Lasiocampidae
Saturniidae
Sphingidae
Notodontidae
(including
Thaumetopoeinae)
Noctuidae
(including
Agaristinae)
Pieridae
Papilionidae
No. of Species Nea retie Pa lea retie Other Duration (y-'s)
12
1
2
1
7
8
1
3
5
1
18
1
5
12
1
6
6
1
2
3
15
1
2
2-17
1
2 2-3
I1 1.5-2
1 1.5-4
22 2-3
1
I3 2-3
1 I4 2-6
I5
3 1.25-7
2
3 1.5-9
3 2 1
2-4
17 7 10 2-6
642 2-6
1 Pectinophora gossypiella (Saunders), diapause recorded in Egypt (Gough, 1916) and
Hawaii (Busck, 1917). The species is believed to have originated from the Indo-
Australian Region.
2 Includes Cydia pomonel/a (L.), which probably is introduced from the Palearctic
(observed by several Nearctic workers and in Yugoslavia).
3 Loxostege frustralis Zeller (Pyraustinae), recorded in South Africa by Broodryk
(1969).
4 Adults of the Australian species Arhodia (l)retractaria Wlk. (Ennominae) were
reared after 21-23 months in diapause (McFarland, in litt.)
5 Family but no species mentioned by Danilevski (1951) in Russia.
environmental changes are genetically variable. A stimulus that elicits
successful development in one species, such as constant chilling for a
certain period, may not be effective in another species or another
population of the same species from a differing climatic zone or eleva¬
tion, or even among all individuals within a population.
Typically, prolonged diapause involves some individuals that wait one
or more full years beyond emergence of their sibs, in populations in
which all individuals enter dormancy, for one of three life cycle pat¬
terns: a) vernal feeding followed by 9 or 10 months dormancy; b) vernal
feeding followed by a few months aestivation and autumnal flight, as in
Hemileuca (Comstock & Dammers, 1937, 1939; Ferguson, 1971), or c)
facultatively double-brooded populations such as in Ethmia semilugens
(Z.) (Powell 1974) and Ant hoc haris (dos Passos & Klots, 1969; Shapiro,
86
J. Res. Lepid.
1981), so that either a few weeks or nearly a full year in diapause
elapses. I also include examples in Tineidae and Cochylidae in which
individuals may wait one year even though sibs have emerged within a
few days, apparently without undergoing any diapause. The potential
for such species to wait more than one season seems likely.
Rearing Methods
Foliage-feeding larvae usually were held in transparent polyethylene
bags lined with folded paper toweling to absorb moisture and provide a
substrate for cocoon construction. If the host plant material was excep¬
tionally susceptible to excess moisture and decay problems, or the moth
species were suspected to use soil for pupation, the lots were placed in
translucent plastic boxes or one-gallon tubs with a few cm of sterile
sand. Thus natural photoperiod normally was available. Prodoxids
were housed in subdued light, in sealed cardboard boxes with a 32— mm
emergence aperture at one end. During 1964—1970 most of the initial
rearing was conducted in a temperature controlled lab (20— 25°C) with
variable humidity (RH 38—48% in dry weather, 52—78% during rainy
periods). Since 1971, the active larval lots have been handled in a
mobile trailer lab on the University of California, Berkeley, campus.
Here minimum temperature was controlled (usually 15-16°C) but not
maximum, and humidity varied with outside air conditions.
Temperature and relative humidity were recorded continuously by
Bendix-Friese hygrothermographs placed on the lab shelving or in
temperature cabinets with the collections or in a weather shelter
located near outdoor cages. During the emergence season, moths were
harvested daily or at 2— 3 day intervals. Prodoxids that failed to remain
in emergence vials and died inside boxes were harvested at irregular
intervals and at the end of each season.
Rearing lot numbers. - A number-letter designation was assigned to
each collection of one or more larvae. It reflects the year and month in
which the collection was made (e.g., JAP 70C8 refers to the eighth lot
recorded in March 1970). The number accompanies all associated
material, including reared moths and parasitoids, preserved larvae and
other artifacts such as pupal shells, and the data in notebooks. The
habitat, hostplant, behavioral, emergence, and preservation data are
summarized in a d-Base II program. Voucher specimens and associated
data are deposited in the Essig Museum of Entomology, University of
California, Berkeley.
Overwintering regimes. - At the end of each season, usually in
October or November, lots known or suspected to contain carryover
larvae or pupae were exposed to one or a combination of two, storage
methods used to manipulate winter temperature conditions:
1. Laboratory: A constant temperature (20° ± 1°C), low humidity
(40—60% RH) room on the U.C. campus, was used for control sublots in
25(2): 83- 109, 1986(87)
87
studies of prodoxids. Other overwintering lots sometimes were left in
the mobile trailer lab, which was unheated for 6 weeks in midwinter
during 1976-1979.
2. Berkeley cage : Many collections were exposed to natural winter
temperature and humidity in outdoor screen cages at the Oxford Tract,
U.C. Berkeley. Cages were provided with a roof, but in windy storms
the containers received direct moisture. Temperatures are moderate at
this coastal station, and did not fall below 0°C during several winters
monitored. Weekly means of daily maximum and minimum tempera¬
tures remained above 10°C during most of the winter. RH fluctuated
daily and seasonally, generally between 50—80% in dry weather,
65—95% during storms.
3. Refrigerator. A kitchen refrigerator without precise temperature
monitor (4° ± 1.5°C) was used for chilling during part of the winter in a
few instances.
4. Russell insectary : An unheated, fully ventilated lab at the U.C.
Russell Reserve near Lafayette, CA, was used to expose prepupal
larvae to uncontrolled winter temperatures and humidity. The site is
situated ca 10 airline km inland from San Francisco Bay, in the Briones
Hills at ca 250 m elevation. Temperatures frequently dropped below
freezing and weekly means of daily maxima and minima ranged ca
+6°C to 11°C in mild winters, -4°C to +7°C in colder winters. These
are much colder conditions than at Berkeley. For example, average
monthly mean temperatures at Russell in 1971-73 ranged from 4.5°C
lower in October to 8.5° and 7.4° lower in December and January than
the 20 -year average at Berkeley.
PRODOXIDAE
Prolonged diapause is documented in most yucca moths (Koebele,
1894; Powell, 1984a, 1984b; Powell & Mackie, 1966; Riley, 1892). I
have recorded emergences of adults following multiannual dormancy in
the prepupal larvae of Parategeticula pollenifera Davis, and in nearly
all the species of Prodoxus and Agavenema. Larvae of Tegeticula have
been observed to survive more than one season; Riley (1892:117) noted
that a large percentage fail to complete development in the first year,
with some of the moths “not issuing until the second, third of fourth
year,” but he did not give specific data or report conditions of over¬
wintering. I carried out extensive tests with 4 Prodoxus species associ¬
ated with Y ucca whipplei in California and Y. schottii in Arizona over a
20— year period. The larvae of these species commonly remain in
diapause 4—8 years in artificial conditions even though neighbors in
the same plant complete development in a prior year. Mass emergence
of a whole colony may wait 6 years, if exposed to constant temperature,
but mortality was significantly higher as compared to year IV (Powell,
1984a); and in one instance mass emergence occurred after 16 and 17
years in diapause (Powell, 1985, unpubl. data).
88
J. Res. Lepid.
Diapause development in Prodoxus aenescens Riley and P. cinereus
Riley is a complex and dynamic process, responding to gradually
changing temperatures, probably coupled with moisture factors. Lar¬
vae held in constant temperature (± 20°C) and natural photoperiod
throughout winter, or exposed to constant temperature chilling (0° to
9°C) for 50 days, remain in diapause, while refrigeration in constant
darkness in gradually decreased (6 weeks), then gradually increased (7
weeks) temperatures at means of 3° to 10°C induced varying propor¬
tions of individuals to develop (Powell, unpubl. data).
The following records are for species that have not been extensively
studied and originate from localities distant from Berkeley, characte¬
rized by extremely different seasonal climates from those the larvae
were exposed to in rearing.
Prodoxus quinquepunctellus (Chambers)
This species is widespread, from Arizona eastward, in association with
an array of yuccas in the Sections Sarcocarpa and Chaenocarpa (Davis,
1967). Larvae were reported by Riley (1892) to sometimes remain in
the dry floral stalks 2, 3, or 4 years, although apparently he did not
observe successful development of carryover individuals. I obtained
delayed emergences of P. quinquepunctellus from three collections
taken in Arizona and New Mexico, the latter over 4-5 year periods. In
contrast to California species of Prodoxus , some individuals developed
even when held in constant temperature.
The first material, consisting of stalks thought to be two species of
Yucca , possibly intermedia and g/az/ca, was collected in late September,
1963, 5 km W of Albuquerque, Bernalillo Co. by J. A. Chemsak (JAP
63J1-J2). A sample of 24 larvae was removed for preservation. The
remainder were held in constant temperature through the following
two seasons, and diapause development occurred in 7 individuals, one
in 1964, 6 in 1965. In November, 1965, half the stalks were transferred
to the Russell insectary, where winter III elicited emergence of 5 P.
quinquepunctellus in 1966. During the same season, the remaining
stalks in the lab produced 6 moths; one more emerged from them in
1967. Thus, development of one or more individuals took place each
year in the lab, 73% of those that emerged (fig. 1). Moths eclosed in
April, 1964, and March to early May in 1965, approximately coincident
with the flight period in the Albuquerque area (Davis, 1967).
A second New Mexico collection was made near Portales, Roosevelt
Co., in late October, 1973, by N. M. Jorgenson (JAP 73K1), and
consisted of current year stalks of Yucca glauca. These were held in my
lab until December 1, then at the Russell insectary over winter, and 40
P. quinquepunctellus responded in diapause development in 1974. In
midwinter, 1974-75, a sample of 12 carryover larvae was removed for
preservation, and the rest of the lot was moved to the outdoor cage at
25(2): 83-109, 1986(87)
89
63JI- J2
20 -
L L R R R
L L
L/R R/B B B B B
70C8 , Cl I
'69 *70 ‘71 ‘72 ‘73 *74 ‘75 *76 '77 '78
FFLRRRR/BBBB
'70 '71 '72 '73
F L R R
Fig. 1 (upper): Successive annual numbers of Prodoxus quinquepunctellus
(Chambers) that emerged from two collections of yucca inflorescence
stalks (see text for data).
(lower): Successive annual numbers of Prodoxus co/oradensis Riley
that emerged from four collections of Yucca schidigera inflorescence
stalks from the Mojave Desert (see text for data).
Overwintering sites: F, in field; B, Berkeley, outdoor cage; R, Russell
Reserve, unheated insectary; L, laboratory at 20 ± 2°C.
90
J. Res. Lepid.
Berkeley, where it was stored for 5 years. Three additional moths
emerged, 2 in 1976 and one in 1978, after 3 and 5 years in diapause (fig.
1).
One additional stalk was collected from Yucca angustissima , 1 km W
of Cottonwood, Yavapai Co., AZ, 30 July 1970, by R. E. Dietz and P. A.
Rude (JAP 70G35). It was retained in the lab for one year, during
which no moths emerged, then transferred to the Russell insectary.
There 26 P. quinquepunctellus successfully completed development, 30
May to 20 June 1972, following the second winter. Only one flaccid-
appearing larva was discovered by splitting the stalk at the end of
1972.
Prodoxus coloradensis Riley
This species feeds in stalks of Yucca schidigera and Y. baccata in
California and in other yuccas of the Section Sarcocarpa in the western
U.S. (Davis, 1967). Collections made in the Mojave Desert, 31 March —
2 April 1970 (Dietz & Powell), indicated that prolonged diapause in
natural populations is commonplace in that habitat.
At a site 8.5 km north of Cottonwood Springs, Joshua Tree National
Monument, Riverside Co., CA, Y. schidigera was in full to late bloom
on March 31, and none was seen with newly emerging inflorescences.
P. coloradensis adults were numerous, yet there appeared to be no
1969 stalks. Dry stalks in the vicinity appeared to originate from 1968;
each had emergence holes along with few to many carryover larvae
(JAP 70C7-8). Because adults ofP. coloradensis had already emerged,
it could not be inferred with certainty that the observed stalks were
older than one year. It was evident, however, that either a substantial
portion of larvae had carried over from 1968 or a previous season, or
that many 1969 larvae had not completed diapause development for
the 1970 season.
At Belle Campground, 32 km to the northwest and 300 m higher than
Cottonwood Springs, Y. schidigera showed no signs of inflorescence
development. Flowering and yucca moths had been observed at this
site in mid- April, 1963, and it was evident that activity would not begin
before mid to late April in 1970. Again, there appeared to be no 1969
stalks, while those from a previous year contained old emergence holes
along with carryover Prodoxus larvae (JAP 70C11), which tended to
confirm our estimate of stalk age at Cottonwood Springs. On the basis
of weathered appearance of the stalks, subsequent vegetative growth,
and lack of prior emergences, Y. schidigera stalks at Ryan Mountain,
Joshua Tree Natl. Mon. (JAP 70C14) and Cedar Canyon, 27 airline
km NE of Kelso, San Bernardino Co., CA, (JAP 70D1), also were
judged to be more than one year old.
The 1970 collections were housed at the Russell insectary beginning
in early April, and no P. coloradensis emerged in 1970, nor in 1971
25(2): 83-109, 1986(87)
91
after transfer to the constant temperature lab over winter 1970—71.
Most moths (82%, n=78) completed development in 1972, following
their first overwintering at the Russell insectary. Additional larvae
were discovered in 70C11 in February, 1974; the lot was retained and
exposed to winters in the cage at Berkeley. Only 2 adults completed
development in the succeeding 2 years, then, inexplicably, 11 P. col-
oradensis (38% of the Belle Campground total, n=29) emerged in April
1977, following a second full winter of drought conditions in Berkeley, 9
years after their larval feeding in 1968 stalks (fig. 1).
It is possible that the 70C14 and 70D1 collections, which originated
from higher or more northern sites than Belle Campgound, were made
sufficiently early (e.g., 4 or 5 weeks ahead of flowering) that develop¬
ment was interrupted; but negative results of all other 1970 collections
including those of P. sordidus Riley (see below) and P. y-inversus Riley
(Powell, 1985) suggested that the 1969—70 winter was one that failed
to elicit diapause development in Mojave Prodoxus generally.
Evidence of 1969 failure in the Y. schidigera inflorescence crop was
dramatic at a site on Black Canyon Road, south of Cedar Canyon. Here
an extensive stand of tree-like Y. schidigera possessed 1969 stalks that
were dry, hard, and black, atrophied before they were fully grown, as
though they were killed by a late freeze. None had any signs of
lepidopterous larval feeding. A number of 1968 stalks were found
containing small numbers of larvae; some had emergence holes left by
sibs that must have faced catastrophe in 1969. A collection (JAP 70D4)
of the pre-1969 stalks produced no adults in 1970 and only one P.
coloradensis in 1972 after overwintering at Russell. Dissections of the
stalks in early 1973, however, revealed a few larvae still in diapause.
Prodoxus sordidus Riley
Moths treated under this name are believed to represent two species
(D. S. Frack, in litt.) associated with Joshua Tree, Yucca brevifolia. It
appears that a species with tan forewings feeds in the inflorescence
scapes, while a whitish moth originates from larvae in pods. However,
some of my stalk-inhabiting larvae produced the pale morph, and more
information is needed to confirm separation of larval feeding niches of
the two. My rearing data are pooled.
Collections at Antelope Valley, 33 km E Gorman, Los Angeles Co.,
CA, March 11, 1963 (Chemsak & Powell, JAP 63C8) just ahead of the
current season flowering, confirmed that prolonged diapause occurs —
most emergences took place in late March and early April, 1963, but 2
P. sordidus completed development in February, 1964 after storage in
the lab. A midwinter collection from 5 km SE Pinon Hills, L. A. Co., 23
December 1969 by P. A. Opler (JAP 70A1) produced only 6 adults after
housing in the lab for the remainder of the season. None emerged in
1971 after winter II in constant temperature, but in 1972, 90 moths
92
J. Res. Lepid.
responded to winter III at the Russell insect ary. Three more individuals
waited until 1973, following a second winter at Russell, and one P.
sordidus emerged in the 6th season, after the material was transferred
to Berkeley in midwinter 1973-74.
The same emergence pattern was shown by population samples made
31 March - 2 April 1970 in the central Mojave Desert, despite the fact
that they were collected after a full winter in the field. One of these
(JAP 70C12) at Belle Campground, Joshua Tree Natl. Mon., Riverside
Co., CA, was made while Y. brevifolia was in full bloom and Prodoxus
was active in low numbers. It was not possible to judge stalk age
precisely, but it appeared at least two seasons growth contained larvae
in diapause; none of these matured in 1970. Three more collections
were made at higher, more northern sites, ahead of 1970 Y. brevifolia
flowering (70D2: Cedar Canyon, 27 airline km NE Kelso, San Bernar¬
dino Co., CA; 70D10: 6 km S of Barnwell, 44 airline km NE Kelso;
70D24: Kyle Canyon, 15 km W Highway 95, 30 airline km WNW Las
Vegas, Clark Co., NV). In each sample, no P. sordidus matured in
1970, nor in 1971 following a year in the constant temperature lab.
Most of the emergence (84%, n=140) occurred in year III following
overwintering at the Russell insectary in 1971-72, while 6 individuals
eclosed in each of the next two years after another winter at Russell
and at Berkeley from midwinter 1973-74. Only one of the collections
(70D10) was retained beyond the 5th year, and 10 P. sordidus de¬
veloped successfully in 1975 after storage over winter in the outdoor
cage at Berkeley, but none matured in the 7th season (fig. 2).
Prolonged diapause would seem less critical to continuity of popula¬
tions in P. sordidus than in other Prodoxus because Yucca brevifolia
blooms more consistently. Nonetheless, combined with observations of
P. coloradensis , the data indicate that certain winters are suboptimal
to diapause termination in Prodoxus in widespread areas of the Mojave
Desert.
Weather records from Twenty nine Palms (15 airline km N of Belle
Campground, at 610 m) and Mountain Pass (35 air km NNW of Cedar
Canyon, at 1450 m) for the preceding 4 and 3 years, respectively,
showed that the 1969-70 winter was unusual, if not exceptional in a
long-term sense. At both stations the rainfall total for October through
March was lower than in any of the preceding few years, 19 mm
contrasted to a 5— year average of 45 mm at Twentynine Palms, and 50
mm vs. a 4— year average of 92 mm at Mountain Pass. Possibly of
greater significance to the moths, the 1969-70 winter was characte¬
rized by unusually mild temperatures. In the 13— week midwinter
period, December through February, monthly means averaged 11.1°C
at Twentynine Palms in 1969—70, contrasted to a range of 8.5— 10.9°
(avg. 9.9°) during the preceding 4 winters; while at the higher station
monthly means averaged 7.0°C in 1969—70, but ranged 3.1 to 6.7° and
averaged only 4.8° during the preceding 3 seasons.
25(2): 83-109, 1986(87)
93
30
70CI2
70D2
20
10
° '70 '71 '72 ‘73 '74
80
60
40
20
F L R R R/B
70DI0
-i
70 7 1 72 73 74
F L R R R/B
70D24
I
7o 7 1 72 73 74 75 76
F L R R R/B B B
70 7 1 72 73 74
F L R R R/B
Fig. 2: Successive annual numbers of Prodoxus sordidus Riley that
emerged from four collections of Yucca brevifolia inflorescence
stalks from the Mojave Desert (see text for data).
Overwintering site designations explained under figure 1.
94
J. Res. Lepid.
Agavenema barberella (Busck)
Agavenema species feed on Agave and display larval habits similar to
those of stalk-inhabiting Prodoxus. The adults are not found in the
flowers of the larval host, as are Prodoxus , and larvae usually occur in
the main scape well below the inflorescence. Collections were made
from various species of Agave in Arizona in 1968—1970. Stalks were
housed at the Russell insectary in 1968—69 and 1969—70 winters, in
the lab 1970—71, returned to Russell in 1971 — 72 and not retained
beyond the fourth season. Development occurred irrespective of the
kind of artificial winter conditions.
Lots collected at Madera Canyon, Santa Rita Mts. in June 1968, prior
to the current season flight, from Agave palmeri (JAP 68F43-44)
(Opler & Powell), produced moths primarily the same season (83% of
those reared, n=130). Emergences occurred from 15 July to 13 Octo¬
ber, and 20 larvae were harvested in late September. Only 7 indi¬
viduals completed development in 1969, after exposure to winter II at
the Russell insectary, followed by none in 1970 and 1971, yet 15 A.
barberella emerged in the 4th season after storage at Russell.
Larvae were collected in Agave schottii at Molino Basin, Santa Catali¬
na Mts., in September, 1969, after the summer activity period (JAP
69J10). Small numbers of moths issued, 5 in 1970, 3 in 1971 (following
a lab winter), and 7 in 1972, after winter III at Russell (47% of the total,
n=15).
Lastly, 7 collections of one-year old or current season stalks were
made from 3 Agave species in central and northern Arizona,1 29 July to
2 August, 1970. All yielded similar results: one or no moths in 1970,
modest numbers in 1971 (19% of the total reared, n=134), despite
having overwintered in the lab, followed by most of the emergence
(78%) in the 3rd season after exposure to winter at Russell in 1971-72.
The normal flight period of A. barberella is poorly known, with
scattered records from March to September in southern Arizona
(Davis, 1967). The flowering phenology of most agaves probably en¬
ables a more protracted activity season by Agavenema within popula¬
tions than is characteristic of yucca moths.
Agavenema pallida Davis
This species, which is closely related to the preceding one and may be
a geographical race, occurs in the deserts of California and Baja
California Norte, Mexico (Davis, 1967; UCB specimens). Its seasonality
is more restricted than that of A. barberella , similar to the California
*JAP 70G30: 4 km E of Peach Springs, Mohave Co., 1969 stalks of Agave utahensis ; 70G31: same
data, 1970 stalks; 70G32: 5 km SW Mingus Mtn. summit, Yavapai Co., 1969 stalks of A. parryi\
70G33: same date, 1970 stalks; 70G36: Molino Basin, Sta. Catalina Mts., Pima Co., 1969 stalks A.
schottii ; 70H6: same data, 1970 stalks; 70H5: 1.5 km NE of Colossal Caves, Pima Co., 1970 stalks A.
schottii (R. E. Dietz, J. Powell and P. A. Rude).
25(2): 83-109, 1986(87)
95
species of Prodoxus. Collections from Agave deserti in March, 8 km E
Jacumba, San Diego Co., CA (JAP 63C31) and April, 1963, Pinyon
Flat, 29 airline km SE of Idyllwild, Riverside Co., CA (JAP 63D10)
revealed prolonged diapause. Carryover larvae remained at the end of
the season, and in 63D10 a few adults emerged in 1964 and 1965
despite housing in the lab during the preceding winters.
Two collections made in Baja California in March, 1972 and 1973,
yielded A. pallida adults in diminishing numbers in years I, II, and III.
A total of 25 moths emerged in year I following overwintering in the
field (51%, n=49), 17 in year II (35%), and 7 in year III (14%), and 2
carryover larvae were discovered in winter IV (JAP 72C12: 8 km E of
El Rosario, 1971 stalk of Agave shawii; 73C5: 5 km S of Rancho Santa
Ynez, 1972 stalks of A. cerulata spp. lnelsoni\ Doyen & Powell).
TINE ID AE: SCARDIINAE
“Scardia” cryptophori (Clarke)
This large gray tineid is widespread in montane western North
America. It was transferred from Morophaga H.-S. to the genus Scar¬
dia Tr. by Davis (1983), who treated Morophaga and its Palearctic type
species as a synonym of Scardia . However, S. cryptophori is structural¬
ly and biologically dissimilar from Nearctic members of Scardia. In
contrast to other Scardiinae and other fungus-feeding Tineidae, this
species is host-specific, feeding in the sporophores of Polyporus ( Cryp -
tophorus) volvatus, which grows on recently dead conifers (Lawrence &
Powell, 1969). This fungus is available throughout the season but
appears to be in a fresh state preferred by S. cryptophori primarily in
spring following winter precipitation and snow melt.
Among numerous collections from the Sierra Nevada and Cascade
Ranges in California, two from Trinity County produced some larvae
that proceeded to maturity without dormancy, as most do, and others
that entered diapause for one year. This suggests that adverse condi¬
tions, particularly desiccation, may prolong diapause.
Four collections of sporophores were made in the vicinity of Hayfork,
Trinity Co. in late May, 1973. Moths (n=36) emerged from all 4 lots
15—25 June, but in two groups (JAP 73E46, E47) a number of larvae
spun cocoons in dry spots remote from the fungus, and most of these did
not emerge. A few cocoons were cut open in September, revealing
carryover prepupal larvae. The lots were stored in boxes at the Russell
insectary. After removal to Berkeley in early June, 1974, 10 M.
cryptophori emerged in late June, one year later than their sibs.
ETHMIIDAE
Ethmia plagiobothrae Powell
This species flies in early spring, primarily in March, in the foothills of
the Coast Ranges and Sierra Nevada in California. The larvae feed on
96
J. Res. Lepid.
flowers of Plagiobothrys (Boraginaceae) a spring annual, and pupae
remain in diapause from the beginning of the dry season until early
spring the following season. I have made numerous collections of
larvae, but they are highly susceptible to disease in rearing, and the
few adults obtained emerged after one year (Powell, 1971). In one
instance (JAP 69D58, Powell, 1971) 10 E. plagiobothrae were reared
after one winter (100% of the emergence) even though the collection
data and rearing conditions were essentially the same as for a collection
of the closely related species, E. scylla Powell, that produced moths 2, 3
and 4 years after pupation (Powell, 1974). In another collection (13 km
SE Three Rivers, Tulare Co., 4 May 1979, JAP 79E24) all 4 adults
emerged the next year, between Feb. 14—27. On two occasions, howev¬
er, pupae were still healthy appearing during the second winter, after
19 and 21 months, but development did not take place (Powell, 1971).
Thus it was not surprising that a collection in 1980 produced one E.
plagiobothrae that delayed until the second spring before emerging.
We found larvae on Plagiobothrys nothofulvus, 6 km S of Rough and
Ready, Nevada Co., CA, on 4 May 1980 (M. Buegler, J. DeBenedictis &
Powell) (JAP 80E17). About a dozen were placed in pill boxes, 2 to a
container with inflorescences and folded tissue paper. After cocoon
construction the boxes were left open inside a translucent plastic box,
stored in the mobile trailer lab at Berkeley through the summer. In
October they were moved to the outdoor cage, but no development
resulted after the first winter. In 1981—82 the material was again
exposed to winter in the cage, and one male emerged between 24
February and 24 March, 1982. Other individuals were unsuccessful in
pupation, succumbing either to disease or desiccation prior to or after
cocoon construction.
Ethmia epileuca Powell
This species was described from the Panamint Range, CA, in the
northern Mojave in 1959 and subsequently has been recorded in the
low deserts of southern California, Baja California, and Arizona
(Powell, 1973; UCB specimens). The foodplant, an annual Phacelia ,
was discovered in 1977, and the one specimen reared spent two years in
diapause.
A few Ethmia larvae were found feeding externally on Phacelia
crenulata (Hydrophyllaceae) at Zzyzx Springs, near Baker, San Ber¬
nardino Co., CA, 20 April 1977 (JAP 77E94). They were provided with
soft paper toweling, but only one E. epileuca successfully constructed
its cocoon. It was stored in a transparent plastic bag in the mobile
trailer lab through summer and fall, then in an outdoor cage at
Berkeley during late winter and spring, 1978, but diapause develop¬
ment did not occur. The cocoon was again placed in the cage for the
1978—79 winter until mid-February, then in the mobile lab. A female
25(2): 83-109, 1986(87)
97
E. epileuca emerged on 2 April 1979 after nearly 24 months in di¬
apause. The 1978-79 winter was appreciably colder than the preced¬
ing year at Berkeley, 190 heating day degrees greater (based on
18.3°C), during October through February.
Interestingly, a related species, E. semilugens (Z.), which has the
capability of developing with a short diapause of a few weeks, of one
year, or of several years (Powell, 1974), also feeds on Phacelia crenulata
(Powell, 1971). Collection records for E. epileuca , however, indicate
that this species has a univoltine cycle with flight in early spring.
Ethmia (Macelhosiella Group) n. spp. A, B
Larvae that proved to be two undescribed species which are structur¬
ally and biologically similar to Ethmia geranella (B. & Bsk.) were
discovered in western Fresno County, CA in March 1975 and collected
again in April 1978. Both species feed in spring, estivate as pupae, and
fly in late fall, as do other members of the Macelhosiella Group. Eggs
hibernate, presumably in diapause or a temperature-dependent quiesc¬
ence (Powell, 1973). In both Fresno County collections, some indi¬
viduals carried over to a second or subsequent autumn; however the
pattern was quite different between the two species, even though they
were reared and held over winter in identical conditions.
Species A: The larva is green with faint longitudinal, gray in-
tegumental shading. The adult is a whitish moth with faint ochreous
along the discal cell, and it differs from other western species of the
group by lacking a hind wing costal penicillus in the male. P. A. Rude
and I collected larvae on Phacelia tanacetifolia (Hydrophyllaceae) at
the Ciervo Hills, 29 airline km SE of Mendota, Fresno Co., CA, 16—18
March 1975 (JAP 75C1) and at Jocalitos Cyn., 9 airline km S of
Coalinga, Fresno Co., 17 March 1975 (JAP 75C2). Larvae were placed
in translucent plastic vials and cardboard pill boxes, 1 or 2 per contain¬
er, with folded tissue and small blocks of yucca scape pith, into which
they burrowed for cocoon construction. Others were confined in trans¬
lucent plastic bags with paper toweling and hostplant material. They
were stored in the mobile trailer lab at Berkeley for the remainder of
spring and early summer; in late July about half the containers were
moved to the Russell insectary, while the remainder were placed in the
outdoor cage at Berkeley in September.
Most of the moths (n=25) emerged in October, 1975. The carryover
cocoons were exposed to winter conditions at Russell during January —
April, 1976, and subsequently were retained in the outdoor cage at
Berkeley. Two adults completed development in October, 1976, and 13
others developed but were trapped in the cocoons and unable to distend
the wings, probably in the first season. No more emerged in 1977 or
1978.
In early April, 1978, following the 1975 — 77 drought, Jocalitos Canyon
98
J. Res. Lepid.
was again a sea of wildflowers, and we made additional collections of
the two Ethmia. Larvae of Species A (78D12) became diseased and
most were preserved for taxonomic study; 7 were retained in translu¬
cent plastic boxes with paper toweling and yucca blocks in the mobile
trailer lab. Four of these emerged as adults 25-30 October 1978. The
remaining 3 carried over and eclosed 10-27 Oct. 1979, after storage
over winter in the outdoor cage at Berkeley.
Thus 29 of 34 successful emergences (85%) of Species A occurred
during the first fall after larval feeding, while the remainder developed
one year later.
Ethmia Sp. B: The larva is irregularly mottled, predominately gray,
with longitudinal bands of orange dorsally and laterally, resembling
that of E. charybdis Powell (Powell, 1971). The adult is dark gray; the
forewing has a trace of ochreous and a variable black line along the
discal crease and a whitish dot at the end of the discal cell, and the male
hind wing has a costal penicillus. Thus the adult is structurally quite
similar to that of E. timberlakei Powell, which feeds on Phacelia
ramosissima in southern California, but the larva of the latter is green
with a yellow dorsal stripe (Powell 1971). Larvae of Species B were
mixed with those of Species A in the field at Jocalitos Canyon in March,
1975, but were outnumbered ca. 10:1. I could not detect a spatial
differentiation on the plants; both fed within the scorpioid floral spikes.
In the lab, larvae were segregated by color and handled in the same
rearing conditions as outlined for Species A.
In marked contrast to the preceding species, no individuals of Species
B completed development in 1975. Instead, all 4 moths that meta¬
morphosed did so after carrying over, two in early November, 1976,
and one each in November 1978 and 1979. The same diapause behavior
obtained in the April 1978 collection at Jocalitos Canyon: about a dozen
larvae were confined, of which none developed in 1978, 2 moths
emerged in October 1979, none the following year, and 2 more in
October, 1981, after 42 months in diapause.
I visited the Jocalitos Canyon site on 21 March 1977, following two
drought years in California, and found the spring vegetation dry; there
had been essentially no germination of annuals. Hence, a large larval
eclosion of Phacelia- feeding Ethmia would have been mostly doomed,
and if prolonged dispause in the pupal stage acts as a buffer against
such disasters, the strategy must be keyed to maintenance of diapause
through autumn preceding a dry spring.
Adults of Species B were taken at blacklights at Jocalitos Canyon on
10 November 1977 (Powell & Rude). There had been no heavy rains in
the region that fall, only ca 6 mm in the Fresno area, less than 1/4 the
normal, by early November; the drought did not end until late Novem¬
ber and December, 1977. This leaves unanswered the question of how
prepupal larvae appraise the potential for spring growth of annual
Phacelia and either maintain diapause or undergo development in
October.
25(2): 83-109, 1986(87)
99
TORTRICIDAE : OLETHREUTINAE
Grapholita vitrana (Walsingham)
Grapholita vitrana was originally described from northern Oregon,
and it is commonly associated with Astragalus (Fabaceae) in sandy
situations along coastal areas of California, on San Miguel and Santa
Catalina Islands, and in interior and coastal areas of Baja California,
Mexico, including Isla Cedros (SDNHM, UCB Specimens). The larvae
feed on green seed in the bladder-like pods of locoweed.
A collection of pods containing larvae of G. vitrana and Everes amyn-
tula (Bdv.) (Lycaenidae) was made from an Astragalus growing on
riverine dunes along the Salinas River near King City, Monterey Co.
on May 3, 1974 (JAP 74E20). The butterflies emerged within a month,
while the tortricids spun tough, papyrus-like cocoons in which prepupal
larvae entered diapause. After drying, the lot was stored in the mobile
trailer lab on the Berkeley campus. Seven G. vitrana emerged between
28 March and 28 April, 1975. The remaining cocoons were left undis¬
turbed and in the same overwintering conditions except without heat
control for 5 weeks in December and January, 1975-76, so were
exposed to temperatures of 2° to 4°C on several occasions. Diapause
development occurred in 4 individuals (2d, 29), and moths eclosed
between 23 March and 11 May 1976. Similar housing of remaining
carryover larvae during the third winter, 1976—77, resulted in 5 more
G, vitrana (2d, 39) emerging, between 26 February and 17 April,
1977, after 33-35 months in diapause.
Diapause extending to a second or third year has been recorded in
several other seed-feeding species of Grapholita and the closely related
genus Cydia (e.g., Dickson, 1949; Hedlin, 1967; Nesin, 1984; Tripp,
1954).
COCHYLIDAE
Cochylis yuccatana (Busck)
This distinctive species is widespread in the southwestern deserts,
from Texas (TL: Nuecestown) to southern California and Baja Califor¬
nia Norte, Mexico (UCB Specimens). The type series was reared from
Yucca haccata\ we have found the larvae in flowers of Yucca brevifolia
in the Mojave Desert, and Agave shawii in coastal Baja California
Norte. There are no records of multiannual diapause, but the species is
capable of either completing development without delay or remaining
dormant until the following year, which suggests a potential for pro¬
longed diapause exceeding one year.
A single larva taken 5 km W of Palmdale, Los Angeles Co., CA, from
Yucca brevifolia in late March, 1968, pupated and produced an adult 15
days after collection (JAP 68C62). Several caterpillars feeding on
Agave near San Telmo, Baja Calif., in mid-March, 1972, did not mature
that spring, but two moths eclosed in late April, 1973, after 13 months
in diapause (JAP 72C6); while another collection from the same host
100
J. Res. Lepid.
near El Rosario, Baja Calif., in late March, 1973, produced larvae of
both types. Five C. yuccatana emerged between 24 April and 8 June,
1973, and one later that summer, and one prepupal larva carried over
to complete development in May or June, 1974 (JAP 73C4). Both
carryover lots were housed at the Russell insectary.
PYRALIDAE: CHRYSAUGINAE
Satole ligniperdalis Dyar
This curious polymorphic and sexually dimorphic species is wide¬
spread in the southwestern Nearctic, from western Texas to the west¬
ern edge of the deserts in California (TL = Portal, AZ). Adults have
been reared from seed pods of Chilopsis linearis (Bignoniaceae) in
southern Arizona and southern California (USNM specimens).
A collection of the linear fruits of Chilopsis was made by J. T. Doyen
on the Kelso Dunes, ca 12 airline km SW Kelso, San Bernardino Co.,
CA, on July 14, 1974 (JAP 74G9). Ten adults of S. ligniperdalis
emerged between 18—27 July, and two more later that fall. Although
several larvae abandoned the pods by late July and the plant material
became badly covered by sooty mould, an apparently healthy larva was
revealed by dissecting its cocoon in February, 1975. The lot was
therefore placed in a cardboard box and stored in the outdoor cage at
Berkeley. Two females emerged in early September, 1975, one on June
25, 1976, and a final one in the fourth season, between October and
December, 1977, after 38—40 months in diapause.
Evidently larvae were fully fed at the time of collection and spent
diapause as prepupal larvae in cocoons. Because they were held in
subdued light and the emergence dates varied by more than two
months after late June, it appears photoperiod was not a primary factor
influencing diapause development.
PYRALIDAE: CRAMBINAE
Loxocrambus sp. near mojaviellus Forbes
A somewhat heterogeneous assemblage of specimens from the low
deserts of California has been designated as a new species with a
manuscript name by A. B. Klots (AMNH). We accumulated large series
of this species in a survey of active dune systems of the Colorado and
Mojave deserts (Powell, 1978). Included was one specimen that re¬
mained unfed, presumably as a prepupal larva in diapause, for 28
months.
The larva was sifted from active dunes south of Rice, Riverside Co.,
CA, Jan. 30, 1977, by J. T. Doyen and P. A. Rude (JAP 77A19). In early
February I opened its sand-covered silken tube to find a large pyralid
larva. The larva evidently was fully fed and did not accept plants in the
lab. It was retained in a dry container with sand in the mobile trailer
25(2): 83-109, 1986(87)
101
lab (unheated 6 weeks in midwinter) until February, 1978, then in the
outdoor cage at Berkeley for one year. Rainfall resulted in wetting the
sand once or twice during the 1978—79 winter. After storage in the
mobile trailer lab again for four months, a somewhat dwarfed male
emerged 1 June, 1979.
GEOMETRIDAE
Eupithecia dichroma - johnstoni group
A single specimen of Eupithecia was reared after spending two win¬
ters in diapause, and although the species identification is question¬
able, the record is noteworthy because prolonged diapause has been
recorded for few geometrids. The moth failed to expand its wings fully
upon emergence, but it seems to match the description of E. johnstoni
McDunnough with only minor differences. The latter species, which
was known only from the type male from Inyo County, CA, at the time
of McDunnough’s revision in 1949, has the whitish ground color on the
forewings more contrasting with the red-brown subbasal and subter¬
minal bands than seems to be true of the deformed reared specimen
from Modoc County, CA. The male genitalia, particularly the unique
aedeagus, confirm a close association with johnstoni and E. rindgei
McDunnough, a paler species described from Plumas County, CA. The
cornutus is lightly sclerotized basally in the Modoc example, a feature
not shown in McDunnough’s (1949) illustrations, but otherwise the
three species are quite similar in this character.
The geometrid caterpillar was collected incidentally along with larvae
of Pyramidobela quinquecristata Braun (Ethmidae) and a polyphagous
tortricid, Sparganothis tunicana (Walsingham), which were webbing
and feeding on inflorescences of Penstemon laetus spp. roezlii (Scrophu-
lariaceae) at Rock Creek, 15 km NE of Adin, Modoc Co., 12 June 1974
(JAP 74F21). Several adults of the Pyramidobela and Sparganothis
were reared within a month; neither of these species diapauses as a
prepupal larva or pupa. In late July I discovered a geometrid pupa in
the material and placed it in a plastic vial with tissue paper. This was
retained in the mobile trailer lab at Berkeley until mid-December, then
transferred to the insectary at Russell for 60 days. Examination indi¬
cated the pupa to be still alive in August, 1975, and it was again moved
to the Russell insectary for overwintering. It was transferred back to
Berkeley on 14 March 1976, and the moth emerged 14 days later, after
ca 21 months in diapause.
SATURNIIDAE
Hemileuca electra (Wright)
This fall-flying, diurnal species occurs in southern California, where
the larvae feed on Eriogonum fasciculatum (Polygonaceae) in spring.
102
J. Res. Lepid.
Summer is passed by pupae in diapause. As noted by Comstock &
Dammers (1939), in captivity the larvae are susceptible to disease and
are difficult to rear.
I collected seven mature larvae at Mission Gorge, San Diego Co., CA,
[ca 8 km W of Santee] on E. fasciculatum , 19 March 1950. None
successfully developed that season, but one pupa held indoors carried
over, and a female eclosed 27 November 1951, after 20 months di¬
apause. The capability of emerging following one summer of dormancy
or delaying until the succeeding or a later autumn may be characteris¬
tic for all species of Hemileuca. It has been recorded for H. maia (Drury)
(Ferguson 1971; W. D. Winter in litt.), H. burnsi Watson (Comstock
and Dammers, 1937), H.juno Packard (Comstock & Dammers, 1939),
and H. eglanterina (Boisduval) (Winter, in litt.) and inferred for others
by Tuskes (1985).
Saturnia mendocino Behrens
This diurnal saturniid occurs in the North Coast Ranges and Sierra
Nevada of California (Ferguson, 1972), south at least to El Dorado Co.
(UCB specimen). The larvae have been recorded by several authors to
feed on Arbutus and Arctostaphylos (Ericaceae); Ferguson suggests
that S. mendocino also feeds on shrubs of other families, apparently
based on circumstantial associations for the closely related species, S.
walterorum Sala & Hogue, in southern California.
David Wagner collected an ovipositing female and egg cluster of S.
mendocino on Arctostaphylos pungens var. montana near Alpine Lake,
Marin Co., CA, during a field trip with our immature insects class, on
April 13, 1979. The female continued to produce eggs for several days;
larvae were reared, May 4 to July 3, 1979, on Arctostaphylos from the
U. C. campus (DLW lot L10— 14— 79). The cocoons were held in an
outdoor cage in a plastic bag with damp moss during the 1979-80
winter. Four adults emerged in May, 1980. The remaining pupae were
left in a drawer at room temperatures, yet produced two more moths in
1981, none the following year, and one S. mendocino finally emerged in
May, 1983, after nearly 4 years in diapause.
Third and fourth year emergence also is recorded in the Palearctic
species, Saturnia pyri (Schiffermiiller), in Maryland (Bryant, 1980).
NOTODONTIDAE
Pheosia rimosa Packard
I discovered two larvae of this widespread species at Rock Creek, ca 2
km SW of Tom’s Place, Mono Co., CA, 26 August 1983, on Populus
trichocarpa (Salicaceae) (JAP 83H122). The caterpillar, which I mis¬
took for Sphingidae owing to the short caudal horn, was described by
Dyar (1891) and others and illustrated in Packard’s monograph, but its
remarkable crypsis seems not to have been mentioned. The larvae are
25(2): 83-109, 1986(87)
103
peculiar compared to most Notodontidae, being naked, gray, with a
greasy or pearly sheen, prominent spiracles and exaggerated interseg-
mental constrictions. They perch during the day, hanging downward,
on the stems of poplar, back of the distal leaves. There they resemble
the older stems, which develop rings of enlarged nodal growth that are
matched exactly in color by the larvae.
The collection was temporarily housed in a plastic bag and trans¬
ported in a field ice box during a trip, and one of the larvae pupated
loose in the bag by August 31. The larva, pupa and foliage were
transferred to a plastic box with sandy soil September 1, but the lot was
allowed to become moldy while stored in the mobile trailer lab at
Berkeley, and the second larva died. In February, 1984, the material
was still damp and the loose pupa on the soil surface was noted to have
a thin bloom of mold on its surface and was presumed dead. It was
placed in a refrigerator (± 4°C) for 5 weeks but did not metamorphose
in that season.
The pupa was left in situ on the soil surface and was refrigerated
during the 1984-85 winter, from October until February. A large,
normally developed female of P. rimosa , which is of the pale morph
characteristic of populations east of the Sierra Nevada in California,
emerged during 16—23 March 1985, after 18 months in diapause. That
is, nearly one year later than presumably would be normal for this
bivoltine species.
NOCTUIDAE
Egira crucialis (Grote)
There appear to be few records of prolonged diapause in Noctuidae,
although many overwinter as pupae. Thus carryover records of Egira
crucialis , for which we do not have accurate emergence dates, seem
worthy of recording, to call attention to the potential for extended
dormancy in noctuids.
Species of Egira Duponchel ( =Xylomyges Gn. and Xylomania Hamp.)
are univoltine and fly in early spring, often at quite cold temperatures.
In central California they are active from late December to May, the
particular flight period varying with the species and elevation. Larvae
feed during spring foliation, and pupae in diapause estivate and hiber¬
nate until midwinter or spring. We have reared only a few of them, but
two E. crucialis remained in diapause beyond the normal spring flight
period.
Evidently Egira crucialis is a general feeder; we found young larvae
on new foliage of Pseudotsuga menziesii (Pinaceae), while previous
records are from hardwoods. Crumb (1956) listed collections from
Alnus (Betulaceae) and Quercus (Fagaceae) in Washington State, and
Prentice (1962) recorded those plant genera as well as Arbutus (Eri¬
caceae) and Salix (Salicaceae) from Vancouver Island, British Col-
104
J. Res. Lepid.
umbia. Our material was taken ca 2 km west of Angwin, Napa Co., CA,
15 May and 1 June, 1979 (DeBenedictis & Powell — JAP 79E62,
79E73). Larvae were reared in polyethylene bags, then transferred to
translucent plastic boxes with sterile soil after ca 3 weeks. Pupae in
soil-encrusted cells were transferred to the outdoor cage in December
and held there until April, 1980. First-year adults should have emerged
by this time because in this area E. crucialis flies from mid-February to
early April. The collections were not given close surveillance after
spring, 1980; they were stored in the mobile trailer lab, without heating
for 6 weeks in midwinter. One dead female E. crucialis was found in the
79E73 lot in early April, 1981, and a dead male in 79E62 in June, 1982.
The circumstances indicated that both emerged during the 1980-81
winter (i.e., after 18-22 months in diapause), while I was away on
sabbatic leave, although the male may have held over an additional
year.
Discussion
Previously unpublished instances of diapause extending one or more
years beyond that believed to be normal in the population are reported
for 19 species of moths, representing 8 superfamilies. Including these,
Table 1 lists taxa for which I have seen records of prolonged diapause in
90 species in 10 superfamilies. This summary is incomplete but reflects
the state of knowledge about the taxonomic distribution of the phe¬
nomenon in Lepidoptera. The preponderance of records in a few fami¬
lies, Prodoxidae, Saturniidae, Pieridae, and Papilionidae, at least in
part indicates rearing efforts, while some taxa such as Geometridae
and Noctuidae may be disproportionately underrepresented owing to
the failure of lepidopterists to look for viable carryover individuals. It is
no coincidence that most of the microlepidoptera listed in Table 1 are
Prodoxidae and Ethmiidae, the two families with which I have worked
most intensively.
While it would be premature to attempt a detailed summary of the
pattern of occurrence of prolonged diapause in Lepidoptera, a few
generalizations seem apparent: a) Dormancy persists beyond the nor¬
mal flight season in prepupal larvae and pupae; it is rare or undetected
in adults, eggs, and early instar larvae, b) It has been observed most
often in cone- and seed-feeding species that depend upon fruit crops of
erratic abundance and in Lepidoptera that live in areas of seasonal
drought, c) The ability to carryover appears to be more prevalent
among certain butterflies and larger moths than in smaller moths.
The generalization that prolonged diapause is more common in Mac-
rolepidoptera may be a picture painted with too broad a brush; more
likely the phenomenon is characteristic of certain taxa, and is rare in
others, within most Ditrysian superfamilies. For example, in the Tor-
tricidae, I have seen records of delayed emergence in 8 species, reported
25(2): 83-109, 1986(87)
105
in 17 references by prior researchers, in addition to the one given here.
All of these are seed-feeding Eucosmini (1 species) and Grapholitini (7
spp.) (Olethreutinae). Although biologies of a large number of Tortrici-
nae have been studied, apparently prolonged diapause has been re¬
ported in none of them. Tortricinae generally and members of the
dominant, worldwide tribe Archipini in particular, tend to be species
that are indiscriminate in feeding preferences and life cycle pattern,
often homodynamic with no fixed dormancy stage. Species that under¬
go diapause do so as eggs or first instar larvae or in adults; it is very
rare in full grown larvae or pupae (Powell, 1964: 17). By contrast, most
Olethreutinae are host specific (6% polyphagous vs. 24% in Tortricinae,
Powell 1980) with a fixed life cycle, and dormancy commonly occurs in
prepupal larvae. Not coincidentally, olethreutines, especially Eucosmi¬
ni, reach their greatest diversity, while tortricines are depauperate, in
desert areas.
On the basis of literature reports and the taxonomic diversity of
prolonged diapause among my rather few rearings of desert species, I
speculate that most oligophagous Lepidoptera in areas of seasonal
drought estivate as prepupal larvae or pupae and that most if not all
are capable of producing a facultative second flight and/or carrying
over to a subsequent season. Because 2—3 year diapause can occur
successfully in tiny moths, such as Coleophora in the Turkistan desert
(Falkovitch, 1973), we may expect that in groups such as Gelechiidae,
which are characteristically diverse in arid and semiarid regions, the
capability of prolonged diapause is not rare. For such insects winter
temperatures may be important mitigators of diapause development,
as in yucca moths, but rainfall has been implicated as critical in some
butterflies (e.g., Emmel, 1975:144, and unpubl. in litt.; Nakamura &
Ae, 1977), as has been documented for various other insects.
Various aspects of diapause and its importance in insect seasonality
have been extensively studied, but the physiological mechanisms of
prolonged diapause are poorly understood (e.g., Tauber et al., 1986).
Presumably particular token stimuli needed to promote the late phases
of diapause maintenance and diapause termination are not received.
Hence, when thermal or other thresholds are reached that would have
resulted in postdiapause development, the diapause maintenance
period continues. The degree of individual variation poses interesting,
as yet unanswered questions; often some individuals metamorphose,
while others exposed to the same stimuli do not. Usually this occurs in
environmental conditions that are abnormal, but such variation indi¬
cates there are differing genetic factors in diapause potential within
colonies, or even among sibs of one egg clutch.
Tauber et al. (1986: 53, 188, 198, 274) have reviewed the role of
prolonged diapause in the evolution of seasonality, life histories and
speciation. In their discussion there is an assumption which has been
made by several authors that extended dormancy regularly occurs in a
106
J. Res. Lepid.
certain proportion of the population as an evolutionary bet-hedging
tactic. Tauber et al. credit me with recognizing that there are two kinds
of prolonged diapause, either a response by whole populations to
adverse conditions by carrying over, or a normal, genetically deter¬
mined occurrence in a certain proportion of the individuals (Powell,
1974). However, I also pointed out that we do not have experimental
evidence to demonstrate that there is a fixed polyphenic expression of
the genotype, wherein a small number of individuals carry over
irrespective of environmental conditions as a kind of buffer against
extraordinary climatic extremes. This is still true; in Lepidoptera we do
not have data to document that populations of any species express this
phenomenon.
In yucca moths ( Prodoxus ) I have convincing evidence that such
genetic predisposition is not the case; under optimum winter environ¬
ments all or nearly all larvae undergo development, while in adverse
conditions all or nearly all maintain diapause (Powell, 1984a, b, 1985).
Multiannual emergence patterns such as reported by Carolin (1971) for
Coloradia (Saturniidae) appear to represent a fixed polyphenism, but
that kind of genetic variability may be manifested only in response to
suboptimal climatic situations. Hence, there may not be two discrete
classes of prolonged diapause. Rather, populations adapted to erratical¬
ly variable seasonal and biotic environments may be composed of
genetically differing individuals such that none, few, many or all
maintain diapause depending upon the degree of fitness to optimum
seasonal conditions. With Prodoxus it is easy to obtain 100% carryover
but almost impossible to promote 100% diapause development under
experimental circumstances in the first year. Later, after several years
in diapause, individuals will respond to environmental cues that were
not sufficient in the first year and proceed through development. This
kind of response, rather than a genetically predisposed calendar of
events that occurs irrespective of external stimuli, may be producing
successive year emergence observed in other insects.
Lepidopterists are urged to record observations such as those given
here, particularly the environmental conditions to which dormant
stages are subjected, as a necessary step toward more detailed analysis
of prolonged diapause.
Acknowledgements. I thank the following, who made many of the larval
collections which led to data presented here: J. A. Chemsak, J. T. Doyen, N. M.
Jorgensen, R. E. Dietz IV, P. A. Opler, and P. A. Rude. The last three were
supported in part by N. S. F. Grant GB-6813X during 1967 — 1970, which
funded field travel during those years. Several people responded to inquiries by
offering unpublished records of carryover pupae and subsequent emergences;
these included R. S. Bryant, Baltimore, MD; J. A. DeBenedictis, Berkeley, CA;
T. C. Emmel, Gainesville, FL; N. McFarland, Sierra Vista, AZ; D. L. Wagner,
Berkeley, CA; and W. D. Winter, Dedham, Mass. Authorities of the Depart-
25(2): 83- 109, 1986(87)
107
ment of Forestry, U. C. Berkeley, and particularly A1 Bianchi, caretaker,
provided facilities at the Russell Reserve, where collections were held for
overwintering during 1965-1976. Identifications of agaves were provided by
H. S. Gentry, Phoenix, AZ and of many other flowering plants by J. L. Strother,
U. C. Berkeley Herbarium. The cooperation of all these and other students and
colleagues is greatly appreciated.
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Journal of Research on the Lepidoptera
25(2): 110-120, 1986(87)
An exceptional case of paternal transmission of the dark
form female trait in the tiger swallowtail butterfly,
Papilio glaucus (Lepidoptera: Papilionidae)
by
J. Mark Scriber1
and
Mark H. Evans
Department of Entomology, University of Wisconsin, Madison, WI 53706
Abstract. The melanic dark and yellow forms of the tiger swallowtail
butterfly, Papilio glaucus glaucus L., are believed to be controlled by a
locus on the Y (W) chromosome. Since the female is the heterogametic
sex (XY) in Lepidoptera, dark females should (and generally do)
produce only dark daughters while yellow females produce only yellow
daughters. Exceptional broods have been reported in which some
yellow females arise from dark, and more rarely some dark females
arise from yellow mothers. Scriber et al (1986) have shown that these
results (as well as both colors of females arising from either colored
mother) can be obtained experimentally by hybridizing and backcros-
sing with the northern subspecies Papilio glaucus canadensis R & J.
The purpose of this communication is to describe the results of a
highly unusual case in which the locus for the dark gene controlling
melanism from a dark female P. glaucus was transmitted by a male in
two separate pairings. This observation has never before been re¬
ported and is significant that it suggests that the locus for black color
is not necessarily totally lost when it (rarely) dissociates from its
normal (Y) chromosome. Since chiasmata at oogenesis in female
Lepidoptera are generally believed to be non-existent, crossing-over is
believed not to occur in female Lepidoptera. While pur results do not
permit us to distinguish between a cross-over event and a non¬
disjunction of the sex chromosome, we nonetheless have observed
results of a rare event, especially for Lepidoptera.
Introduction:
The melanic dark and yellow forms of the tiger swallowtail butterfly,
Papilio glaucus glaucus L., are thought to be controlled by a locus on
the Y (W) chromosome (Clarke and Sheppard, 1959, 1962). In fact, this
locus controlling dark morph expression in female P. glaucus is one of
1 Current address (and reprint requests to): Dept, of Entomology, Michigan State University, East
Lansing MI. 48824
25(2): 110-120, 1986(87)
111
but a few sex-linked marker genes in butterflies (Robinson, 1971;
Soumalainen, 1973; R. Hagen, 1986, and pers. comm.). The female is
the heterogametic sex in Lepidoptera, and dark females should (and
generally do) produce only dark daughters, and yellow females produce
only yellow daughters. Exceptional broods have been reported (Ed¬
wards, 1884; Clarke and Sheppard, 1959, 1962; Scriber et al., 1986) in
which some yellow females arise from dark, and more rarely some dark
females arise from yellow mothers. Scriber et al. (1986) have shown
that these results (as well as both colors of females arising from either
colored mother) can be obtained experimentally by using hybrids with
the northern subspecies Papilio glaucus canadensis R & J. Intermedi¬
ate colored females with a “peppered” or “sooty” color over the yellow
tiger-striped background are also observed in nature (see Edwards,
1884; Clark and Clark, 1951), and have been experimentally produced
by hybridization or backcrossing with P. rutulus or P. g. canadensis
(Clarke and Willig, 1977; Clarke and Clarke, 1983; Scriber et al, 1986).
In addition to the partial or complete suppression of the Y-linked
melanism in female P. glaucus when paired to P. rutulus and P. g.
canadensis males (Scriber et al., 1986), it has also been suggested that,
if the Y chromosome bearing the locus for the dark gene is occasionally
lost during meiosis of dark females, yellow daughters would be pro¬
duced (Clarke and Sheppard, 1962; Clarke et al., 1976). Scriber et al.
(1986) describe such a case in which loss of the locus for dark color in F2
hybrid females is likely to have occurred. However these authors have
also observed cases of yellow hybrid daughters of dark mothers
which retain the locus for black color. Depending on the male used in
subsequent matings, all yellow, all black, or both colors can be obtained
from these yellow hybrid or yellow backcross females (Scriber, 1985;
Scriber et al., 1986).
Here we describe the results of a highly unusual case in which the
locus for the dark gene controlling melanism in female P. glaucus
seems to have been transmitted by a male to two different hand-
pairings. This situation has never before been reported and is signi¬
ficant in that it suggests that the locus for black color is not necessarily
totally lost when it (rarely) dissociates from its normal (Y) chromosome.
Since chiasmata at oogenesis in female Lepidoptera are generally
believed to be absent, crossing-over is believed not to occur in female
Lepidoptera (Haldane, 1922; Robinson, 1971; Clarke and Sheppard,
1973; Soumalainen et al., 1973; Turner and Sheppard, 1975). However
a suspected crossover in the supergene controlling female polymorph¬
ism in Papilio memnon L. has been reported (Clarke and Sheppard,
1977).
Our recent studies of the genetic basis of dark morph expression in
Papilio glaucus have involved hand-pairings and mass-rearing of
thousands of individuals derived from various geographic locations
across North America (Scriber and Evans, 1986a). All of these and the
112
J. Res. Lepid.
following specimens are maintained in the Papilio research collection
of J.M.S. at the Department of Entomology at Michigan State
University.
Results.
A near-normal but slightly melanic or “sooty” (Fig. 1) yellow male
adult butterfly was obtained from a normal-appearing dark morph
mother (#674) which was field-captured in Adams County, Ohio by M.
H. Evans and W. W. Warfield on July 1983. This male eclosed in 1984
and was hand-paired on May 14, 1984 (#1129) to a virgin yellow morph
female (P. g. glaucus) which was lab-reared from a yellow morph Ohio
female (#631) field-captured on 14 May, 1983. On the following day
(May 15, 1984) a second pairing (#1132) using the same male was
made to a virgin P. g. canadensis female (which was lab-reared in 1983
from a 25 June, 1983 field-captured yellow female from Barron County,
Wisconsin). All subsequent larvae were reared through to pupation
under identical controlled environment conditions (16/18 photo/
scotophase, corresponding thermoperiod of 23 V2°C/19 V2°C). Pupae
were weighed and adults were permitted to eclose in cylindrical screen
cages.
To our surprise, we observed dark as well as the expected (yellow)
females in the progeny of both crosses (Table 1). According to all
understanding to date, dark females were not expected to occur in
offspring of either of these pairings. We have never before observed
dark daughters in the lab-reared offspring of more than 600 different
P. g. canadensis mothers. While it is possible that Papilio glaucus
larvae could be accidentally introduced with foodplant leaves in our
laboratory mass rearing procedures at Madison, this is unlikely and
careful precautions are continually made to prevent this possibility. We
Table 1. Special case in which an aberrent-colored male mated to two
different yellow females resulted in dark female daughters
(Madison, Wl, 1984).
Females Pupae
Total eclosed remaining
pupae Males -
Mating reared eclosed Yellow Dark Dead Alive
Parentage* number (n) (1984) (1985) (1984/1985) (1984/1985) (n) (1986)
OH(Y) x OH(D)* 1129 69 32 2 9 3 16 1 2 4
PgcxOH(D)* 1132 82 40 4 12 0 21 0 3 2
* Female parent listed first. The OH(D) parent represents an aberrent-colored male (see
Fig. la and 1b) reared in 1983 from a normal appearing dark morph mother (#674)
captured in Adams County, Ohio on 8 July, 1983. This male was mated to a yellow
daughter of an Ohio P. g. glaucus yellow female #632 on 14 May, 1984 (mating #1129);
and to a daughter of P. g. canadensis female #614 on 15 May, 1984 (mating #1132).
25(2): 110-120, 1986(87)
113
have not observed any such occurences in the last 5 years with nearly
120,000 ova in our lab. Such errors cannot possibly account for the 38
dark females produced from these two pairings.
Discussion.
We interpret the results as evidence of male transmission of the gene
controlling black color (which is found on the Y chromosome of the
heterogametic female). The sons of pairings 1129 and 1132 were all
normal in appearance (i.e. they were not black or dark colored as the
female morph can be). Approximately 2/3 of the daughters were dark
morph and 1/3 yellow morph, and none of the daughters exhibited
partial color or mosaic patterns (e.g. dark with irregular blotches/
patches of yellow background showing; see Scriber et al, 1986). This
suggests that all cells of dark daughters contain the gene for black
color, and favors the idea of non-disjunction or a cross-over of this locus,
rather than a particulate cytoplasmic explanation (see Clarke and
Sheppard, 1959, 1962).
FOLLOWING PAGE CAPTION:
Fig. 1. Offspring of dark female #674 from Adams Co., Ohio, 1983: a) dorsal
and b) ventral of "slightly aberrant" male (wt. 1.1642); c) dorsal and
d) ventral of a "normal" sibling (wt. 1.0459). This first (aberrant) is
the male parent in crosses 1129 and 1132 (see Table 1), and is our
suspected "carrier" of the female melanism locus.
Fig. 2. Ft hybrid offspring of pairing #1132 (a virgin daughter of a 1983
Barron Co., Wisconsin P. g. canadensis female x the aberrant male,
wt. 1.1642, of Fig. la & b). a) dorsal and b) ventral of a "slightly
aberrant" male (wt. .9386) and c) dorsal and d) ventral of a normal
sibling male (wt. .8522).
Fig. 3. Offspring of an F2 pairing (#1695; see Table 2) of a dark daughter and
a slightly aberrant male (shown in Fig. 2a, 2b) both derived from
pairing #1132 (Table 1). a) dorsal and b) ventral of an aberrant male
(wt. .9410), and c) dorsal and d) ventral of a normal male sib (wt.
1.0416).
Fig. 4. Female offspring of a cross between a yellow morph P. g. glaucus x
the "aberrant" male (cross #1129): a) dorsal and b) ventral of a
typical dark morph, (wt. 1.4010) and of a typical yellow morph c)
dorsal d) ventral (wt. 1.3700) sibling (see Table 1).
Fig. 5. Female offspring of Fn hybrid cross of a P. g. canadensis x "aber¬
rant" male P. g. (cross #1132). a) dorsal and b) ventral of a typical
dark morph (wt. 0.6964), and c) dorsal and d) ventral of a typical
yellow morph (wt. 0.6755) sibling (see Table 1).
Fig. 6. A wild collected "aberrant" male from Dane County, Wisconsin
(collected 10 August 1983).
114
J. Res. Lepid.
illllllilllHIli
25(2): 110-120, 1986(87)
115
liiimmum
116
J. Res. Lepid.
Under the hypothesis of a non-disjunction as a causal mechanism, we
could expect our male to be of the genotype X (XYD), where the “Y”
represents the Y chromosome carrying the gene for dark color. The P.
g. canadensis and yellow morph P. g. glaucus females would both be of
the genotype XY, and offspring (1129 and 1132; Table 1) would be
expected to be the following: XX and X (XYD) males, XY yellow
females, and Y (XYD) dark females. This explanation would account for
the occurrence of both dark and yellow female daughters; however so
would the hypothesis of a cross-over event.
In a cross-over of the locus for dark color in this species we would
expect the male parent of 1129 and 1132 to be of the genotype XDX.
When paired to the P. g. canadensis female and the yellow morph P. g.
glaucus female (both presumably XY genotype) we would expect the
following: XXD and XX males, XY yellow females, and XDY dark
females.
Both the cross-over hypothesis and the non-disjunction hypothesis
provide explanations for observed yellow and dark daughters. Howev¬
er, neither explains the observed deviation from an expected 50:50
ratio of female morphs. Similarly, the reason for the melanism being
restricted to only (some) daughters and none of the sons of this male
carrier (not expressed in himself or his sons) is unresolved for both
hypotheses. We did, however, notice a slight “sootiness” or semi¬
melanism in the generally normal tiger-striped yellow background
proximally on the dorsal surface of the wings in this original male
parent (Fig. 1) and in one of his 44 sons (Fig. 2). We had hoped that this
could prove to be a phenotypic marker for the male black locus carriers
reflecting the X (XYD) or the XXD genotype (from either a non¬
disjunction or a crossover, respectively).
Subsequent pairings with offspring of pairings 1129 and 1132 (Table
1) have yielded poor results. Nonetheless, when the aberrant male son
(shown in Fig. 2) was mated to one of his sisters (pairing 1695; Table 2)
one of the resulting 5 male F2 hybrid sons was markedly melanic in the
proximal 1/3 of the wings (Fig. 3a, b).
Female offspring resulting from pairings #1129 (P. g. glaucus x P. g.
glaucus ) and #1132 (P. g. canadensis x P. g. glaucus) are typical dark
or typical yellow in color pattern (Figs. 4 and 5) with one exception,
where one daughter is a “dark intermediate’. It should be noted that
the female progeny of cross 1129 are larger than those of 1132,
reflecting the genetic differences in size between P. g. canadensis and
P. g. glaucus. It is also noteworthy that the dark females of cross #1132
represent the only known case of melanism being expressed in Fx
hybrids from a P. g. canadensis mother (Fig. 5).
In an attempt to follow up the genetic explanation of our unique
results in pairings 1129 and 1132, (Table 1), we hand-paired male,
yellow female, and dark female offspring of both crosses. Twenty-one
different yellow and dark females from cross 1132 were hand-paired
25(2): 110-120, 1986(87)
117
Table 2. A 1984 F2 hybrid pairing of a dark female and slight aberrant male
(both from pairing 1132; Table 1).
Females
eclosed
Total Males - Pupae
Mating pupae eclosed Yellow Dark alive
Parentage number reared (1984) (1985) (1984) (1985) (1984) (1985) (1985 October)
(1 132*)2 1695 10 2 3 1 0 1 1 2
* Male with aberrant
color; dark morph female
Table 3. Pairings of a yellow female Ft hybrid and two of her dark daughters
(Madison, Wl; 1985).
Females
eclosed
Total Males - Pupae
Mating pupae eclosed Yellow Dark alive
Parentage number reared (1984) (1985) (1984) (1985) (1984) (1985) (1985 October)
1 129(Y) x Pgg*
*wild Wl male
2343
(see
below)
204
— 37 —
6
— 90
71
2343(DK) x
Pgg*
*wild OH male
2957
88
— 35 —
0
— 37
16
2343(DK) x
Pgg*
*wild OH male
2974
81
— 35 —
0
— 36
10
(with copulations of 30 minute durations or more). These pairings
resulted in only 8 females which produced eggs, only two of which
produced any larvae (#1695 produced 34 larvae, #1542 produced 1
larva). The single most useful cross of these attempts was #1695 — an
F2 hybrid of a dark female from 1132 x her aberrent male sibling; see
Figs. 2a, 2b. This cross generated both yellow and dark daughters as
expected under the crossover/non-disjuction hypotheses (Table 2).
Since none of his normal-type siblings (see Figs. 2c, 2d) produced
female daughters from fourteen mating attempts, we are unable to
evaluate whether this aberrent color in males is indicative of possession
of the female melanism gene (i.e. a “carrier” criterion).
Seven different females from cross #1129 were also hand-paired, of
which only 3 produced eggs and only one (pairing #2343 in 1985)
produced any larvae. This backcross of a yellow morph female (from
1129) to a wild Wisconsin P. g. glaucus male resulted in 310 larvae,
which produced 204 pupae. Unfortunately, instead of resolving the
genetic explanation of the paternal transmission of the melanism
118
J. Res. Lepid.
capacity, cross #2343 has become an enigma. This cross involving a
yellow mother produced 90 dark daughters, 6 yellow daughters and 37
sons (Table 3). The existence of dark daughters was totally unexpected
under our hypotheses of crossover and/or non-disjunction because this
female parent (XY) should have produced only yellow daughters. Two
subsequent pairings of her dark daughters (#2957 and #2974; also in
1985) to wild male P. g. glaucus from Ohio yielded the expected all dark
female offspring and an equal sex ratio (Table 3; cf Scriber et al, 1986).
We had hoped that the matings in the 1985 season would clarify our
suspected crossover/non-disjunction hypotheses, but this was not the
case. At present, we have no explanation for the appearance of dark
daughters in pairing 2343 (Table 3). The yellow mother from cross 1129
(Table 2) would presumably have been dark if she possessed the gene
for melanism, since any autosomal suppressor in P. g. canadensis
would not be involved in any pure P. g. glaucus lineage (Scriber et al.,
1986) . However, we are not absolutely certain that the Adams County
(Ohio) population is free of P. g. canadensis genes from the Appa¬
lachian Mountain region (e.g. Ritland and Scriber, 1985; Scriber and
Hainze, 1986).
Conclusions.
We must emphasize that although we cannot prove a crossover or
non-disjunction event, we nonetheless have observed the transmission
by a male of the dark morph trait to his daughters (from a mating with
a Wisconsin P. g. canadensis yellow female, and from a mating with an
Ohio P. g. glaucus yellow female). We do not feel that this phenomenon
(appearance of dark daughters from yellow mothers of two different
subspecies) is likely to be explained by autosomal melanism suppressor
effects from P. g. canadensis introgression. This would require that
both the yellow Ohio female and the yellow northern Wisconsin female
(the female parents in Table 1) were the result of P. g. canadensis
introgression into an ancestrally dark stock. This possibility may not be
as farfetched as initially assumed (see Scriber and Evans, 1986a and
1986b). Another remote explanation is that the wild Wisconsin male
used in pairing #2343 was simply another independent example of a
crossover/non-disjunction, which would also explain dark daughters
from a yellow mother presumed to lack the gene for melanism. In this
regard it is interesting that partially melanic males (e.g. Fig. 6; and
compare Figs. 1, 2, and 3) have been captured from the same popula¬
tion in Wisconsin as the mated male in cross 2343. None have been
tested for the dark gene transmission potential however.
Should we be correct in assuming that our results reflect some form of
crossover in female Lepidoptera, then there should be special precau¬
tions taken by systematists who employ maternal DNA (maternal
inheritance of DNA) techniques in evaluating phylogenies, and assume
a clear record of the maternal lineage (see Avise and Lansman, 1983
25(2): 110-120, 1986(87)
119
for further discussion). The adaptive significance of achiasmatic
meiosis (and the assumption that this is accompanied by the absence of
crossing-over) are not entirely clear, but it has evolved repeatedly in at
least 10 major groups of animals (White, 1973). Sexual mosaics, color
mosaics, and bilateral gynandromorphs of Papilio glaucus may be more
common than generally believed, especially near suspected hybrid
zones (Clarke and Clarke, 1983; Scriber and Evans, 1986b). Perhaps
such chromosomal/developmental abnormalities will provide us with
other additional opportunities to evaluate our crossover/non¬
disjunction hypotheses in the future.
Acknowledgments. This research was supported in part by grants from the
National Science Foundation (DEB #7921749, BSR #8306060, BSR
#8503464), the USDA (#85CRCR-1-1598), the Graduate School and College
of Agriculture and Life Sciences (Hatch 5134) of the University of Wisconsin,
Madison. We especially thank William Warfield for his assistance in the field
and Sir Cyril Clarke, Robert Hagen, and Sarah Rockey for their comments on
the manuscript.
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AVISE, J. C. & R. A. LANSMAN. 1983. Polymorphism of mitochondrial DNA in
populations of higher animals, pp. 147-164 In (M. Nei and R. K. Koehn,
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CLARK, A H. & CLARK, L. F„ 1951, The butterflies of Virginia. Smithsonian Inst.
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CLARKE, C. A. & F. M. M. CLARKE, 1983, Abnormalities of wing pattern in the
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CLARKE, C. A. & SHEPPARD, P. M., 1959, The genetics of some mimetic forms of
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CLARKE, C. A. & SHEPPARD, P. M., 1962, The genetics of the mimetic butterfly,
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CLARKE, C. A. & P. M. SHEPPARD, 1973, The gentics of four new forms of the
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CLARKE, C. A. & SHEPPARD, P. M., 1977, A new tailed female form of Papilio
memnon L. and its probable genetic control. Systematic Entomology
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glaucus L. Nature, 263:585-587.
CLARKE, C. A. & WILLIG, A., 1977, The use of a-ecdysone to break permanent
diapause of female hybrids between Papilio glaucus L. Female and Papilio
rutulus Lucas male. J. Res. Lepid. 16:245—248.
EDWARDS, W. H., 1884, The butterflies of North America (Vol. II). Houghton
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HAGEN, R. H. 1986. The evolution of host plant use by the tiger swallowtail
butterfly, Papilio glaucus. Ph. D. Thesis. Cornell Univ., Ithaca, N. Y. p. 297.
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HALDANE, J. B. S., 1922, Sex ratio and unisexual sterility in hybrid animals. J.
Genetics 12:101-109.
RITLAND, D. B. & J. M. SCRIBER., 1985. Larval developmental rates of three
putative subspecies of tiger swallowtail butterflies, Papilio glaucus , and
their hybrids in relation to temperature. Oecologia 65:185-193.
ROBINSON, R., 1971, Lepidoptera genetics. Pergamon, Oxford.
SCRIBER, J. M., 1985, The ecological and genetic factors determining geographic
limits to the dark morph polymorphism in Papilio glaucus. Bulletin of the
Ecological Society of America 66:267.
SCRIBER, J. M. & M. H. EVANS., 1986a. The genetic control and ecological factors
affecting the North American distribution of melanic (dark morph) poly¬
morphism in female tiger swallowtail butterflies (Papilionidae: Lepidop¬
tera). Ecology (in prep.).
SCRIBER, J. M. & M. H. EVANS., 1986b. Bilateral gynandromorphs, sexual mosaics,
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Journal of Research on the Lepidoptera
25(2): 121-135, 1986(87)
The Phenetics and Comparative Biology of Euphilotes
enoptes (Boisduval) (Lycaenidae) from the San
Bernardino Mountains
Gordon F. Pratt & Greg. R. Ballmer
Entomology Department, University of California, Riverside, CA 92521
Abstract. Euphilotes enoptes larvae in the San Bernardino moun¬
tains utilize both perennial and annual Eriogonum species. Many San
Bernardino mountain locations have the same Eriogonum species;
despite this their utilization as hosts varies amongst populations.
Seasonal flight periods which correspond to the initiation of the major
host’s bloom were not only variable amongst populations, but from
year to year. One spring emerging population did not fly during 1984
and 1985 and another had shortened flight periods. Despite differ¬
ences in hostplants and flight periods, these populations appear to be
more closely related in larval setation to each other than to six other
described subspecies.
Introduction
Populations of Euphilotes enoptes (Boisduval) are widely distributed
in western North America. They can be found in a variety of habitats
from sea level to over 11,000 feet, and from moist cool climates in the
Sierra Nevada mountains to the hot dry desert around Palm Springs.
The nine described subspecies of this small blue (Miller and Brown,
1981) are often better defined by geographic distribution, flight period,
and host plant selection than by adult morphological characters. Dis¬
tribution of certain subspecies can be quite large as in E. enoptes
ancilla (Barnes and McDunnough) covering the seven states, (Califor¬
nia, Colorado, Idaho, Montana, Nevada, Oregon, and Wyoming) or
extremely small as in E. enoptes smithi (Mattoni) which is found only
along the coast of Monterey Co., California (Shields, 1977). The larvae
oiE. enoptes feed exclusively on blossoms of various Eriogonum species.
Most subspecies are known to utilize a single host plant species in a
given location and all are believed to be univoltine with the flight
season coinciding with the onset of the host flowering period. Various
populations fly in every month from March to October.
In southern California two subspecies, E. enoptes dammersi (Com¬
stock & Henne) and E. enoptes mojave (Watson & Comstock) are
recognized. The former flies in late summer and fall in the mountains
and foothills of the Colorado and eastern Mojave deserts; its larval
hosts are Eriogonum davidsonii Greene, E. elongatum Benth., E.
wrightii nodosum (Small) Reveal, and E. w. wrightii (Torr.) S. Stokes.
122
J. Res. Lepid.
Euphilotes e. mojaue flies in the spring in the Mojave Desert and
western fringe of the Colorado Desert; its larval hosts are the annuals,
E. pusillum Torr. and E. reniforme Torr. & Frem. Shields (1975)
speculated on the basis of similarities in distribution and male genitalia
that these subspecies are closely related to each other. The life histories
of both subspecies have been published (Comstock & Henne, 1965;
Comstock, 1966) but the larval descriptions lack sufficient detail to
differentiate them from each other or even other lycaenid species. The
present study is an effort to better define the ecological and evolution¬
ary relationships of these 2 taxa and to compare them with other
named and unnamed montane populations of E. enoptes.
The San Bernardino Mts. are an extremely complex and interesting
geological area. Here the Mojave and Colorado deserts, the coastal
chaparral, and the cooler, moister higher elevations of the mountains
all meet. Along the northern and northeastern slopes occur spring
flying populations of E. enoptes. The northwestern slopes have late
summer populations. In the high elevations there are populations that
fly in early summer and, depending on rainfall patterns, can be found
through mid October. Along the eastern slopes there are populations
that fly exclusively in the fall.
Materials and Methods
Studies of E. enoptes in the San Bernardino Mountains entailed
numerous field observations at four colony sites (figure 1) to determine
seasonal activity, host range, and larval behavior. Doble (DB), el. 6700’,
(2,000 meters) located at the northeastern end of Baldwin Lake, is an
open gently sloped flat of rocky clay soil. The major vegetation consists
of short ground cover perennials with scattered Pinus monophylla
Torr. & Frem. and Artemisia tridentata Nutt. A second locality (AC)
about ten miles (16 km) south-southeast of DB is situated along the
steep slope east of Arrastre Creek (AC), el. 7100’ (2,200 meters). This
site is open with scattered Juniperus occidentalis Hook, P. monophylla ,
Ceanothus cordulatus Kell, Cercocarpus ledifolius Nutt., and a diverse
but sparse community of smaller annuals and perennials; the soil is
rocky and porous. A third locality about 12 miles west of DB at Big
Pines Flat (BP), el. 6800’ (2,100 meters), has uneven terrain with P.
monophylla and Pinus ponderosa Dougl. ex P. & C. Lawson forming
open stands interspersed with scattered low perennials and annuals.
The fourth locality, Mojave River Forks (MR), el. 3100’ (950 meters), is
25 miles (40 km) west of DB at the northwestern corner of the San
Bernardino Mountains. This site is warmer than the other sites. It is a
gently sloped alluvium cut by numerous shallow washes and intermit¬
tent creeks; vegetation is diverse, containing elements of Mojave De¬
sert, montane forest, and coastal chaparral communities. Major
vegetation includes Juniperus californica Carr., Artemisia tridentata ,
25(2): 121-135, 1986(87)
123
Victorville
San Jacinto Mountains
Figure 1 . Map of the study sites in the San Bernardino Mts, abbreviations as
in the Materials and Methods. Line shows 5,000 ft. elevation of
mountains.
and Quercus wislizenii A. Dc. with scattered thickets of Adenostoma
fasciculatum H. & A., Ceanothus spp., and Cercocarpus betuloides
Nutt, ex T. & G. Each of these sites except BP was visited several times
during the years 1983 to 1985.
Larvae of E. enoptes were also acquired from the following 18 sites
(see fig. 2) for comparison of setal characters:
(BG) Bob’s Gap, N. base San Gabriel Mts., Los Angeles Co., Ca., el.
4000’ (1200 meters), 22. V. 83., on E. pusillum GRB; {E. e. mojave )
(CC) Chino Canyon, San Jacinto Mountains, Riverside Co., Ca., el.
2600’ (800 meters), 27. IX. 83., on E. davidsonii and E. w. nodosum ,
GRB & GFP; (Type locality for E. e. dammersi )
(CS) Upper Centennial Spring, Coso Range, Inyo Co., el 6100’ (1900
meters), 1. VIII. 83., on Eriogonum nudum Dougl. ex Benth., J. F.
Emmel; (subspecies undefined)
(EP) El Paso Mountains, vie. Last Chance Canyon, Kern Co. Ca., el.
2500’ (760 meters), 19. V. 83., on E. nudum , GRB & GFP; (undefined
subspecies near E. e. mojave)
(LH) Landels Hill Big Creek Reserve, Monterey Co., Ca., el. < 100’ (30
meters), 17, VIII. 84., on Eriogonum parvifolium Sm. in Reese, GFP;
(E. e. smithi)
124
J. Res. Lepid.
Figure 2. Map of the collection sites; abbreviations as in the Materials and
Methods.
(MA) Marina, Monterey Co., Ca., el. < 100’ (30 meters), 22. VII. 83. on
Eriogonum latifolium Sm. in Reese, GRB; (E. e. smithi)
(MCA) Big Morongo Canyon, Riverside and San Bernardino Cos., Ca.,
el. ca 2000” (600 meters), 17. IV. 84., on E. pusillum, GFP; ( E . e.
mojave )
(MCS) same data as above except 15. IX. 84., on Eriogonum elonga-
tum Benth., GPP; (E. e. dammersi )
(MY) Mayer, Yavapai Co., AZ., el. 4500’ (1400 meters), 15. X. 82., on
E. w. wrightii, GRB; (E. e. dammersi )
(PM) Pyramid Mountain, San Jacinto Mountains, Riverside Co., Ca.,
el. 6000’ (1800 meters), 17. VI. 82., 6 VI. 83., 1. VII. 83., 26. V. 84., on
E. davidsonii, GRB & GFP; (subspecies undefined)
(PR) Point Richmond, Contra Costa Co., Ca., el. < 100’ (30 meters),
23. VII. 83., on Eriogonum nudum auriculatum (Benth.) Tracy ex
Jeps., GRB; (E. e. bayensis )
25(2): 121-135, 1986(87)
125
(PV) 28 mi. E. of Pine Valley on HWy. 8, San Diego Co., Ca., el. 3500’
(1100 meters), 26. VII. 84., on E. elongation, GRB; ( E . e. dammersi )
(RN) Randsburg, Kern Co., Ca., el. 3500’ (1100 meters), 19. V. 83., on
E. pusillum, GRB & GFP; (E. e. mojave )
(SP) Santa Paula, Ventura Co., Ca., el. 1000’ (300 meters), 20. VI. 84.,
on E. parvifolium, GFP; ( E . e. tildeni )
(ST) Stanton, Yavapai Co., Az., el. 3500’ (1100 meters), 15. X. 82., on
E. w. wrightii, GRB; (E. e. dammersi )
(WA) Warren Canyon, near Tioga Pass, Mono Co., Ca., el. 9000’ (2700
meters), 17. VII. 83., on E. nudum, GRB & GFP; (E. e. enoptes )
(WC) Wildhorse Canyon, Mid Hills, eastern Mojave Desert, San Ber¬
nardino Co., CA., el. 4000’ (1200 meters), 2. X. 82., on E. w. wrightii,
GRB & GFP; (E. e. dammersi)
(WW) Wrightwood, 1 mi. W., Los Angeles Co., Ca., el. 6000’ (1800
meters), 7. IX. 82. and 13. VIII. 83., on E. nudum saxicola (Heller) S.
Stokes, GRB & GFP; (Shields, 1977, places populations from this area
in the nominate subspecies but they may be closer to E. e. tildeni)
Larvae were obtained by beating host plant inflorescences, searching
for floral shelters, or by rearing from ova. Ova and larvae were often
found with other lycaenid species including Celastrina argiolus (Lin¬
naeus), Hemiargus ceraunus gyas (W. H. Edwards), Icaricia acmon
(Westwood & Hewitson), Icaricia neurona (Skinner), and Strymon
melinus Hubner. Ova of E. enoptes were easily distinguished by their
poorly defined chorionic ridges, and larvae were separated by setal
outlines. Although color can be variable, larvae of E. enoptes are
usually yellow or white (never green) with pink or red chevron mark¬
ings while larvae of the other species are often green. Samples of larvae
from all localities were injected with Kahle’s fluid, fixed in hot water,
and stored in 80% ethanol.
Often larvae were reared on host plants from their collection sites;
occasionally, other hosts were substituted. Since E. enoptes larvae are
cannibalistic they were reared individually in screened vials with
flower stalks placed in water to maintain freshness; flowers were
frequently changed to avoid mold. Most larvae were permitted to
pupate in soil or the rearing container. Pupae were kept under a
variety of conditions, as shown in Table 1. Eclosion dates were re¬
corded.
As with most Lycaenids, mature (fourth instar) larvae (Langston and
Comstock (1966) and Arnold (1983) state that E. enoptes hayensis and
E. e. smithi respectively have 5 instars, yet in hundreds of rearings of
various E. enoptes populations we have found only four instars of E.
enoptes) are covered with short secondary setae and possess a variable
number of more prominent (longer and erect) setae grouped in loca¬
tions where primary setae should occur (sensu Hinton, 1946) (Fig. 3).
These locations are dorsal (just lateral to the midline), subdorsal
(slightly dorsal to the line of spiracles), and lateral (along the lateral
fold). Also, on the prothorax, a few prominent setae occur on the shield
126
J. Res. Lepid.
Table 1. Pupae initially kept at 27-35°c were refrigerated (5°c) for at least
two months ending in December; afterwards they were kept at
22-27°c. Pupae initially kept at 22-27°c were refrigerated from
Dec. 22, 1983 to April 3, 1984 and returned to 22-27°c. Those
pupae not refrigerated first year were refrigerated with other
pupae their second year for 2-3 months. Those pupae not refri¬
gerated were subjected to moderated daily fluctuations in
temperature. The number of pupae from each site is shown in
parenthesis.
Pupae kept
at 27 — 35°c
Pupae kept
at 22-27°c
Pupae not
refrigerated
first year
Pupae not
refrigerated
AC (4)
BG (5)
MY (1)
BP (5)
EP (7)
BP (9)
ST (1)
MR (3)
LH (25)
CC (3)
WC (3)
DB (54)
McA (15)
DB (8)
SP (3)
McS (65)
EP (8)
MA (1)
PM (7)
MR (5)
PV (2)
PM (1)
PR (9)
PV (6)
WA (2)
WW (3)
ABD 1 *7
Figure 3. Diagram of an E. enoptes mojave larva showing the positions of
the setae counted for the 11 characters. Those positions are (D)
Dorsal, (SD) Subdorsal, (L) Lateral, (ABD 1-7) Abdominal
Segments 1 to 7, and (Shield) Prothoracic Shield.
25(2): 121-135, 1986(87)
127
and many more are located in front of the shield and ventrolateral to
the shield in poorly defined groups. Elsewhere, prominent setae occur
in specified locations and are most abundant on the mesothorax. No
apparent difference in number of prominent setae was found among
abdominal segments 1-6 but an increase in number of lateral pro¬
minent setae was often noted on the remaining segments. No promin¬
ent dorsal setae occur on the seventh abdominal segment in the region
of Newcomer’s organ (honey gland); also none occur on the more
posterior segments.
Both the number and size of prominent setae vary. For comparative
purposes the total prominent setae in each location (both sides of the
larva) were summed for each segment. Prominent setae were given a
value of one if they were at least twice (>0.2 mm) as long as surround¬
ing secondary setae and one-half if they were 1.5—2 times (0.15—0.2
mm) as long as the secondary setae.
Prominent setae in eleven locations were quantified and subjected to
statistical analysis using Duncan’s Multiple Range Test. These loca¬
tions were: (1) prothoracic shield, (2) dorsally on the mesothorax, (3)
dorsally on the metathorax, (4) dorsally on abdominal segments 1-6,
(5) subdorsally on the mesothorax, (6) subdorsally on the metathorax,
(7) subdorsally on abdominal segments 1—6, (8) laterally on the
mesothorax, (9) laterally on the metathorax, (10) laterally on abdomin¬
al segments 1—6, and (11) laterally on abdominal segment 7. Promin¬
ent subdorsal setae on abdominal segment 7 and prominent lateral
setae on abdominal segments 8-10 may offer characters for statistical
analysis but were not included.
A variable number of larvae were used to represent each population;
the minimum number was 6 the maximum 30. Consecutive genera¬
tions of larvae were sampled at DB in June (DB1) and July (DB2) 1983.
Samples were taken from MR in September 1982 (MR1) and October
1983 (MR2). These populations were compared statistically to ascertain
the stability of mean character states. For the populations PM and
WW, larvae from consecutive generations were pooled.
Tables 2-5 present the results of statistical analysis. Populations are
listed according to specified abbreviations followed by the number of
larvae (n), character mean, standard error, and results of Duncan’s
Test at the 1% error level.
Results
Larval setation analysis separates the E. enoptes populations studied
herein into 4 basic groups. The populations of E. e. mojave (MCA, BG,
RN) have the largest mean number of prominent setae. The number of
prominent setae for these populations is significantly higher than for
all other populations in dorsal, subdorsal, and lateral positions. With
population EP they also have a significantly higher mean number of
prominent setae on the prothoracic shield.
128
J. Res. Lepid.
Population EP ranks next in mean number of prominent setae in the
same locations. It differs significantly from all other populations in
prominent setae dorsally on all segments (Table 2) and laterally on
abdominal segments 1 — 7 (Tables 3 and 5). EP and PM together differ
significantly in prominent subdorsal setae on the metathorax (Table
2).
Populations CS, PM, and WA often rank together with means higher
than all other populations except those above. They are not significant¬
ly different from each other in mean number of prominent dorsal setae
on all segments and prominent subdorsal setae on abdominal segments
1—6. PM and WA differ significantly from other populations in promin¬
ent lateral setae on abdominal segments 1—6; they differ significantly
from each other, but not from CS, in prominent subdorsal setae on the
mesothorax and prominent lateral setae on the metathorax. PM and
CS differ significantly from each other but not from WA in lateral
prominent setae on abdominal segment seven.
There is little overall difference in mean number of prominent setae
among the populations AC, DB1, DB2, BP, CC, LH, MA, MR1, MR2,
MY, PR, PV, SP, ST, WC, and WW. For all setal characters they either
do not differ significantly from each other or form a series of overlap¬
ping nonsignificant subsets. Populations DB1 and DB2, which repre¬
sent consecutive generations in June and July, respectively, differ
slightly, but not significantly, for all means, except subdorsal setae on
abdominal segments 1-6; these are identical. Populations MR1 and
MR2, which represent consecutive generations at MR in 1982 and
1983, respectively, differ slightly but not significantly for all means
except prominent dorsal setae on the metathorax and dorsal and
subdorsal setae on abdominal segments 1-6; these are identical.
Character means for the San Bernardino Mountains populations,
(AC, DB1, DB2, BP, MR1, MR2), generally do not differ significantly.
However, the mean number of prominent setae on the prothoracic
shield is significantly higher for AC than for DB2 and MR2. Also, DB1
differs significantly from MR1 and BP in mean number of prominent
dorsal setae on the mesothorax; it also differs significantly from MR1 in
mean number of prominent lateral setae on the metathorax and from
both MR1 and MR2 in mean number of prominent lateral setae on
abdominal segment seven.
According to field observations (Table 6) there are at least three
separable populations of E. enoptes in the San Bernardino Mts. The one
at AC is single brooded and can be found only in the spring. Another
population (BP and MR) occurs as adults during late summer and early
fall. At DB E. enoptes appears in early spring, but can be found,
depending on rainfall, into early fall overlapping the flight periods of
the two other populations. The rainfall patterns also affected AC and
MR over the three years. The spring of 1983 was wet, whereas both
1984 and 1985 were seasonably dry. This may account for adults
25(2): 121-135, 1986(87)
129
emerging up to 2 weeks earlier at DB and MR, and both larvae and
adults at AC absent during 1984 and 1985.
Weekly visits to MR during 1982 and 1983 revealed no E. enoptes
adults or larvae prior to August 21 except three larvae on E. pusillum
(29. V. 1982) which had similar setation to E. e. mojaue larvae from BG,
MCA, and RN. Although E. elongatum and E. wrightii trachygonum
normally do not bloom until August, E. dauidsonii is abundant at MR
and blooms from spring to summer. However, the only lycaenid larvae
found on E. dauidsonii at MR were I. acmon.
The eclosion dates for pupae from the four San Bernardino Mountain
sites correspond to field observations. All pupae from DB failed to
diapause. Of four AC pupae, initially kept at 27— 35°C, one failed to
diapause, while the other 3 eclosed within four weeks after removal
from refrigeration in January 1984. Three of five pupae from BP did
not diapause at 27-35°C. The remainder were kept at unheated
Riverside temperatures from December 1983 until they eclosed in July
and August 1984. Nine other BP pupae were kept at 22-27°C, and
refrigerated from December 28, 1983 to April 3, 1984. They eclosed
from May 30, 1984 to July 27, 1984. Five MR pupae were refrigerated
and incubated with those from BP, and eclosed July 9, 1984 to Sept. 2,
1984. Another three MR pupae were not refrigerated but kept at 27°C,
as with those from BP, and eclosed mid July to mid August 1984.
All three pupae from MY, one from ST, and five from WC eclosed
during September and October 1983. In 1984 (after refrigeration treat¬
ment) two more from WC eclosed in July and August; one pupa each
from ST and WC still remained in diapause.
A variable number of pupae from most locations eclosed within four
weeks when initially kept at 27-35°C. These include those from the
San Bernardino Mountains, as noted above, DB (50), EP (2), LH (21),
MCA (3), MCS (4), PM (1), SP (3), WA (3), and WC (2). Of the pupae
initially kept at 22— 27°C only those from PV (6), WA (2), and DB (8),
failed to diapause.
Many pupae eclosed within 4—5 weeks after removal from refrigera¬
tion in December. These include EP (5), MCA (12), and PM (5); one
pupa from PM did not eclose in the winter of 1983 but, after a second
season including refrigeration again, eclosed in January 1984.
Larvae of E. enoptes were found on five species of Eriogonum in the
San Bernardino Mountains. Eriogonum dauidsonii is an annual which
begins to bloom in spring and may continue into summer and fall,
depending on soil moisture. It is the only apparent host oiE. enoptes at
AC and may be the preferred host at BP, since about twice as many
larvae were found on it as on E. wrightii subscaposum. This plant is
absent from DB. At MR it blooms primarily in spring. Eriogonum
kennedyi, which occurs in a few isolated sites in the San Bernardino
Mountains, begins to bloom in May or June; at DB it bloomed during
May and June to September during 1983. In 1984 at DB it bloomed
130
J. Res. Lepid.
Table 2. The mean total prominent dorsal setae on the mesothorax, meta¬
thorax, and abdominal segments 1 through 6; means followed by
the same letter are not significantly different at the 1% level.
Locality
n
meso¬
thorax
mean
S.E.
1*
meta¬
thorax
mean
S.E.
1*
A
1-6
mean
S.E.
1*
MCA
23
8.04
0.54
A
4.41
0.53
A
19.37
1.37
A
EC
17
7.18
0.51
A8
3.88
0.44
A
19.76
1.20
A
RN
19
6. 58
0. 43
8
4.21
0.38
A
21.11
1.41
A
EP
16
4.72
0.44
C
1.78
0.35
6
10.33
1.59
6
itffi
12
3. 42
0.29
D
0.00
0.00
c
0.00
0.00
C
PM
17
3. 24
0.39
D
0.42
0.19
c
2.44
0.88
C
CS
14
3.07
0.21
D
0.00
0.00
c
0.00
0.00
C
BL1
23
1.08
0.23
EF
0.09
0.06
c
0. 13
0.13
C
SP
6
1.17
0. 48
EF
0.00
0.00
c
0.00
0.00
c
Uk
16
1.08
0.27
EF
0.00
0.00
c
0.00
0.00
C
PR
26
0.98
0.20
EF
0.00
0.00
c
0.00
0.00
c
BL2
17
0.91
0.26
EF
0.00
0.00
c
0.00
0.00
c
MRS
22
0.57
0.21
EF
0.00
0.00
c
0.00
0.00
c
AC
8
0.21
0.21
F
0.00
0.00
c
0.00
0.00
c
LH
30
0.37
0.13
F
0.00
0.00
c
0.00
0.00
c
CC
7
0.29
0.29
F
0.00
0.00
c
0.00
0.00
c
8PF
14
0.28
0.15
F
0.00
0.00
c
0.00
0.00
c
MY
9
0.22
0.22
F
0.00
0.00
c
0.11
0.11
c
ICS
27
0.20
0.10
F
0.00
0.00
c
0.00
0.00
c
ST
13
0.19
0.05
F
0.00
0.00
c
0.05
0.03
c
WC
21
0.05
0.03
F
0.00
0.00
c
0.00
0.00
c
PV
15
0.03
0.03
F
0.00
0.00
c
0.00
0.00
c
MR1
17
0.03
0.03
F
0.00
0.00
c
0.00
0.00
c
MA
10
0.00
0.00
F
0.00
0.00
c
0.00
0.00
c
Table 3. The mean total prominent sub-dorsal setae on the mesothorax,
metathorax, and abdominal segments 1 through 6; means follow¬
ed by the same letter are not significantly different at the 1 % level.
Meso¬
meta-
abd.
thorax
thorax
seg.
Locality
n
mean
S. £.
1*
mean
S.E.
1*
1-6
S.E.
1*
MCA
23
7. 80
0.64
A
4.28
0.28
A
12.80
1.69
A
RN
19
7.21
0.41
A
4.74
0.30
A
10.63
1.39
A
86
17
6. 76
0.65
A
4.41
0.41
A
11.47
1.29
A
EP
18
4.67
0.29
B
2.22
0.11
B
1.33
0.62
B
PM
17
4. 24
0.32
B
1.86
0.30
B
1.06
0.69
B
CS
14
3.50
0.39
BC
0.75
0.20
C
0.00
0.00
B
WA
12
2.50
0.15
CD
0.08
0.06
c
0.00
0.00
B
DBi
23
2.48
0.24
CD
0.43
0.15
c
0.00
0.00
B
D62
17
2.29
0.28
CDE
0.32
0.18
C
0.00
0.00
B
AC
8
2.13
0.30
CDE
0.56
0.30
c
0.00
0.00
B
MR2
22
1.80
0.26
DE
0.09
0.09
c
0.00
0.00
B
CC
7
1.79
0.46
DE
0.00
0.00
c
0. 00
0.00
B
MY
9
1.78
0.32
DE
0.00
0.00
c
0.00
0.00
B
PV
15
1.77
0.19
DE
0.07
0.07
c
0.00
0.00
B
ST
13
1.69
0.29
DE
0.00
0.00
c
0.00
0.00
B
MR1
17
1.56
0. 31
DE
0.00
0.00
c
0. 12
0.07
B
LH
30
1.52
0.20
DE
0.00
0.00
c
0.00
0.00
B
MCS
27
1.44
0.21
DE
0.00
0.00
c
0.00
0.00
B
PR
26
1.44
0.14
DE
0.00
0.00
c
0.00
0.00
B
WW
18
1.31
0.19
DE
0.03
0.03
c
0.00
0.00
B
MA
10
1.20
0.29
DE
0.00
0.00
c
0.00
0.00
B
WC
21
1.17
0.19
DE
0.00
0.00
c
0.02
0.02
B
SP
6
1.17
0.65
DE
0.00
0.00
c
0.00
0.00
B
BP
14
0.89
0.27
E
0.00
0.00
c
0.00
0.00
B
25(2): 121-135, 1986(87)
131
Table 4. The mean total prominent lateral setae on the mesothorax, meta¬
thorax, and abdominal segments 1 through 6; means followed by
the same letter are not significantly different at the 1% level.
Locality
n
ffleso-
thorax
Mean
S. E.
lU
meta-
thorax
mean
S.E.
lit
abd.
seo.
1-6
S.E.
lit
wa
IS
10.83
0.37
A
6.75
0.37
AB
12.29
1.26
C
LH
30
10.05
0.AS
AB
3.88
0.A2
CDEF
0.95
0.32
D
MCA
S3
9.91
0.6A
AB
8. A3
0.5A
A
A3. 28
2.95
A
cs
1A
9. BA
0.39
ABC
5.1A
0.31
BC
5.36
1.38
D
£P
16
9.33
0.63
ABCB
6.78
0.A6
AB
30.06
2.65
B
RN
19
9.26
0.21
ABCD
7.A7
0.39
A
A6.53
1.76
A
SP
6
9.00
0.26
ABCDE
A. 25
0.60
CDE
0.00
0.00
D
BG
17
8.76
0.28
BCDE
7.35
0.23
A
A3.2A
1.A9
A
MA
10
8.50
0.5A
BCDE
A. 10
0.55
CDE
0.10
0. 10
D
PR
SB
8.0A
0.30
BCDEF
A. 58
0.A1
CD
0.73
0.38
D
BP
1A
7.79
0.58
CDEF
3.00
0.50
DEFGH
1.A6
0.5A
D
Ml
18
7.50
0.AA
DEFG
3.06
0.A5
DEFG
0.6A
0.30
D
PM
17
7.00
0.33
EFG
5.00
0.33
C
16.71
1.69
C
DBS
17
7.00
0.23
EFG
2.A1
0.38
EFGHI
0.88
0.A6
D
DB1
S3
6.%
0.29
EFG
3.07
0.27
DEFG
2. 17
0. 79
D
MRS
SS
6.A5
0.A2
FGH
1.18
0.A2
HIJ
0.05
0.05
D
MR1
17
6.18
0.5A
FSH
2. 12
0.51
FGHIJ
0.00
0.00
D
AC
8
6.13
0.35
FGH
2.13
0. A0
F6HIJ
0.63
0.30
D
MY
9
6.00
0.87
FGH
0.67
0.A7
IJ
0.00
0.00
D
CC
7
5.71
0.57
GH
0.29
0.18
J
0.00
0.00
D
PV
15
5.67
0.31
GH
0.90
0.32
IJ
0.07
0.07
D
MCS
S7
5.65
0.26
GH
1.69
0.26
GHIJ
0.00
0.00
D
WC
21
A. 86
0.A8
H
0.A3
0.16
J
0.00
0.00
D
ST
13
A.5A
0.A9
H
0.69
0.26
IJ
0.00
0.00
D
Table 5. The mean total prominent setae on the prothoracic shield and
laterally on abdominal segment 7; means followed by the same
letter are not significantly different at the 1% level.
setae setae
on shield abd.seg. 7
Locality
n
mean
S.E.
1*
mean
S.E.
1*
RN
19
3.A7
0. 19
A
7.58
0.50
A
BG
17
3.12
0.23
AB
7.A1
0.37
A
E?
18
2.72
0. 2A
AB
i J. 3*5
0.5A
B
MCA
23
2. A8
0. 15
B
7.98
0.3A
A
PM
17
1.71
0.2A
C
3.A7
0. A2
C
WA
12
1.67
0. 22
C
2.58
0.19
CD
WW
16
1.39
0.20
CD
0.67
0. 23
EFG
AC
8
1.38
0.38
CD
0.63
0.32
FG
PR
26
1.23
0.17
CDE
1.06
0. 17
EFG
CS
1A
0.93
0.22
CDEF
1.86
0.23
DE
DB1
23
0.91
0.21
CDEF
1. A3
0.18
EF
MA
10
0.70
0.21
DEFG
0.50
0.27
FG
MR1
17
0.68
0.21
DEFG
0. 12
0.12
G
BP
1A
0.57
0.20
DEFG
0.A6
0.19
FG
LH
30
0.53
0.1A
EFG
0.97
0.19
EFG
DBS
23
0.53
0.17
EFG
1.06
0.22
EFG
SP
6
0.33
0. 33
FG
0.33
0.21
FG
WC
21
0.2A
0.10
FG
0.00
0.00
G
MR2
22
0.18
0.08
FG
0.09
0.09
G
CC
7
0.1A
0. 1A
FG
0.29
0.16
FG
MCS
27
0.11
0.06
FG
0.19
0.08
6
PV
15
0.07
0.07
G
0.17
0.09
G
ST
13
0.00
0.00
6
0.00
0.00
G
MY
9
0.00
0.00
6
0.11
0.11
G
132
J. Res. Lepid.
Table 6. The weeks of each month on which L — larvae or A — adults were
observed at the 4 different San Bernardino Mt. sites.
MAY JUNE JULY AUGUST SEPTEMBER OCT.
3
4
1
2 3 4
1 2 3 4 1 2 3
4
1
2
3 4 1
AC: 1983
AA L
L L
BP: 1983
L
1985
L
DB: 1983
AL
A
AL AL
A
1984
AL
AL
1985 A
AL
MR: 1983
A
A
AL
AL L L
1984
L
L
1985
A
A
L
during May and June and again in September after summer rains.
Eriogonum wrightii subscaposum, which is common and widespread
above 5000’ in the San Bernardino Mountains, blooms from August to
October. This plant is utilized by E. enoptes at BP and DB. Eriogonum
wrightii trachygonum , which is common mostly below 5000’, also
blooms from August to October. This plant is utilized by E. enoptes at
MR. Eriogonum elongatum , a common species below 5000’, especially
along the southern slopes of the San Bernardino Mountains, blooms
primarily from August to October. It is the major host of E. enoptes at
MR.
The presence of the aforementioned hosts does not always correspond
to the presence of E. enoptes. At MR no E. enoptes larvae were found on
E. davidsonii ; nor were any found on E. wrightii at AC. Both of these
plants are common at many sites in the San Bernardino Mountains
where E. enoptes has not been found. Eriogonum elongatum and E.
nudum , which is utilized by E. enoptes in the adjacent San Gabriel
Mountains, are widespread and abundant at many sites along the
southern slopes of the San Bernardino Mountains yet no populations of
E. enoptes are known to utilize them there. Eriogonum umbellatum
Torr., another common species above 6000’, is a preferred host for some
populations of both Euphilotes battoides (Behr) and E. enoptes , but is
utilized by neither in the San Bernardino Mountains. In fact, E. enoptes
larvae from MR die when fed the local E. umbellatum munzii (Reveal)
as do larvae of E. battoides glaucon (Edwards) (J. F. Emmel, personal
communication), which utilizes another subspecies of E. umbellatum in
the Sierra Nevada.
25(2): 121-135, 1986(87)
133
Observations of larval behavior were noted for several populations of
E. enoptes. In the field, larvae from LH, MR, SP, WW, AC, and PM,
often tie together dry and partially consumed flowers to create loose
shelters within the host inflorescence. At Morongo Canyon (MCS)
mostly first and second instar larvae, rather than later instars, as
expected, were found on the host E. elongatum from September 15 to
November 24, 1984. Under laboratory conditions, these larvae ma¬
tured to third and fourth instars. The larvae fed nocturnally and
remained concealed at the base of host plants by day; they made no
floral shelters. Field evidence (the lack of mature larvae on blossoms)
suggests that larvae from CC and PV may have a similar behavior.
Discussion
Adult eclosion has two determining factors: conditions which termin¬
ate diapause, and thermal summation for subsequent development.
Pupae which break diapause simultaneously may eclose at different
times in the field due to different temperature regimes (in their
environments). Euphilotes enoptes pupae from some populations break
diapause in response to warming after cold treatment, while others
may break diapause in response to other conditions, perhaps indepen¬
dent of cold treatment. When reared under the same conditions, early-
flying populations eclose soon after the end of refrigeration, indepen¬
dent of the time of year, while late-flying populations do not eclose until
several weeks or months later. Both types of diapause occur in the San
Bernardino mountains and one population is facultatively multi voltine.
A high temperature regime (27— 35°C) during development is more
conducive to breaking diapause (or inhibiting its induction) in E.
enoptes than is a lower temperature regime (22-27°C). This has been
shown in other insects as well (Chapman, 1971). Other E. enoptes
populations (PV and WA), in addition to the Doble population, appear
to be at least bivoltine, as indicated by their pupae failing to diapause
when kept at 22— 27°C.
Conditions which Induce diapause in the multivoltine DB population
are not known, but probably are related to host plant condition and/or
moisture stress. Some E. enoptes pupae can also diapause for more than
one year. Termination of diapause in these populations may be affected
by rainfall patterns, temperature, and/or photoperiod.
Various populations of E. enoptes utilize several species of Eriogonum
in the subgenera Eucycla and Ganysma (Reveal, 1969). In the San
Bernardino Mountains E. enoptes utilizes at least four Eriogonum
species belonging to both subgenera and often more than one in a given
locality. However, not all available hosts are utilized nor are the
acceptable hosts utilized wherever they occur. Thus, the distribution of
E. enoptes in this area is largely independent of availability of hosts.
Euphilotes e. mojave may have the most restricted diet of the E.
134
J. Res. Lepid.
enoptes subspecies. So far it has been found only on E. pusillum and E.
reniforme even at sites where other hosts occur, as at BG where E.
davidsonii grows along side E. pusillum. Larvae of E. e. mojave from
MCA collected on E. pusillum , which would switch to E. reniforme in
the lab would not feed on E. davidsonii or E. nudum. Yet larvae of E.
enoptes from MR2 collected on E. elongatum easily switched to E.
davidsonii, E. pusillum and E. microthecum.
First and second instar E. enoptes remain within host plant infloresc¬
ences. Third and fourth instars, from some populations, often create
shelters by tying blossoms together with silk, where they remain until
mature or until food is depleted. Older larvae of E. e. dammersi at
Morongo Canyon do not make floral shelters but probably conceal
themselves at the plant base by day and feed on blossoms nocturnally,
or crepuscularly. Similar behavior may also occur in some other popula¬
tions of E. e. dammersi.
Setation patterns of mature larvae vary among populations of E.
enoptes. These patterns are relatively constant from generation to
generation and offer reliable characters for comparing different popula¬
tions. Many populations (E. e. bayensis, E. e. dammersi, E. e. enoptes, E.
e. smithi, and E. e. Tildeni) have very few prominent setae. E. e.
enoptes larvae have few prominent setae dorsally and dorso-laterally,
but a relatively large number laterally on all segments. Larvae of E. e.
mojave have far more prominent setae than the other subspecies in
nearly all body regions. This permits them to be readily distinguished
from the others.
Larvae of populations of E. enoptes in the San Bernardino Mountains
more closely resemble setal patterns of E. e. dammersi than E. e.
mojave , both of which occur nearby. At sites where both E. e. mojave
and another subspecies of E. enoptes occur, as at Mojave River Forks
and Morongo Canyon, there is no apparent dilution of larval characters
in either. Therefore, it seems unlikely that any gene mixing occurs. Of
course, in both cases their flight seasons are widely separate.
The similarity in larval setation of the San Bernardino Mountain
populations suggests that these are closely related. San Bernardino
Mountains populations of E. enoptes are more-or-less intermediate in
setal characters between the E. e. dammersi populations to the east
and populations of E. e. bayensis, E. e. smithi, and E. e. tildeni to the
west.
General Conclusions
Larval hostplant and setation characters can be utilized to consistent¬
ly separate certain populations of subspecies of E. enoptes from others.
Among the other subspecies (at least E. e. dammersi, E. e. smithi, E. e.
tildeni, and the San Bernardino Mountains populations) host plant
specificity and seasonal flight period are variable from location to
25(2): 121-135, 1986(87)
135
location. The plasticity of these characters may render them unreliable
as indicators of subspecific relationships.
Acknowledgments. The authors wish to express their gratitude to John F.
Emmel for supplying E. enoptes from Upper Centennial Spring and his know¬
ledge of Euphilotes populations. Particular thanks also to Andrew C. Sanders
for plant identifications. Thanks to David Wright for careful reading of the
manuscript and helpful suggestions. Rudolf H. T. Mattoni also provided helpful
suggestions and guidance to the Santa Paula site.
Literature Cited
ARNOLD, R. A. 1983. Conservation and management of the Endangered Smith’s
Blue Butterfly, Euphilotes enoptes smithi (Lepidoptera: Lycaenidae), J. Res.
Lepid. 22: 135-153.
CHAPMAN, R. F. 1971. The Insects Structure and Function, American Elsevier
Publishing Company, Inc. N. Y., 819 pages.
COMSTOCK, J. A. 1966. Life History of Philotes mojave (Lepidoptera: Lycaenidae).
Trans. San Diego Soc. Nat. Hist. 14: 133-136.
COMSTOCK, J. A. & C. HENNE. 1965. Notes on the Life History of Philotes enoptes
dammersi. Bull. So. Calif. Acad. Sci. 64: 153 — 156.
HINTON, H. E. 1946. On the Homology and Nomenclature of Lepidopterous
Larvae, with Some Notes on the Phylogeny of the Lepidoptera. Trans. Roy.
Ent. Soc. London 97: 1 — 37.
LANGSTON, R. L. & J. A. COMSTOCK. 1966. Life History of Philotes enoptes hayensis
(Lepidoptera: Lycaenidae). Pan Pac. Ent. 42: 102-108.
MILLER, L. D. & F. M. BROWN, 1981. A Catalogue/Checklist of the Butterflies of
America north of Mexico. Lepid. Soc. Mem. no. 2.
REVEAL, J.L. 1969. A Revision of the Genus Eriogonum (Polygonaceae). Ph. D.
dissertation, Brigham Young Univ., Univ. Microfilms, Inc., Ann Arbor,
Michigan, 546 pages.
SHIELDS, 0. 1975. Studies on North American Philotes (Lycaenidae) IV. Taxono¬
mic and Biological Notes, and New Subspecies. Bull. Allyn Mus. 28: 1-30.
- , 1977. Studies on North American Philotes (Lycaenidae) V. Taxono¬
mic and Biological Notes, Continued. J. Res. Lepid. 16: 1-67.
Journal of Research on the Lepidoptera
25(2): 136-145, 1986(87)
A New Genus and Species from the Southwestern United
States (Noctuidae: Acontiinae)
Richard M. Brown
323 Calvert Ct., Antioch, California 94509
Abstract. The species albiciliata Smith (1903) is removed from the
genus Cobubatha Walker 1863, and made the type of a new genus,
Allerastria. The genitalia of albiciliata are described, apparently for
the first time. Three new taxa are described in the new genus, two
subspecies of albiciliata ( paula , from the San Joaquin Valley, Califor¬
nia, and chacoensis, from the Chaco Canyon National Monument,
New Mexico) and a new species ( annae from southern California). All
species and subspecies are figured and diagnosed.
Introduction
In 1977 I took a long series of Cobubatha albiciliata (Smith) at the
western mouth of Titus Canyon, on the valley floor of Death Valley
National Monument. Mixed with this series was a short series of moths
that could not be assigned to albiciliata and is described as new. With
the borrowing of additional material and the investigation of the other
species of Cobubatha a number of characteristics were found that
separated albiciliata and the new species from Cobubatha.
From the time albiciliata was described in 1903 by Smith, it has had
uncertain placement. Smith (1903) stated “the species is not really an
Yrias , but it resembles that genus in general form and may remain
here until further material makes a better reference possible.” Barnes
and McDunnough (1912) in their description of the synonym bifasciata
were not certain of the generic assignment when they placed “the
species for the present in Eustrotia” McDunnough described Nerastria
in 1937, and moved albiciliata to that genus in 1938. Most recently
Franclemont and Todd, in R. W. Hodges et al (1983) placed Nerastria as
a synonym of Cobubatha Walker (1863). Based on the charaters
described below, I feel that albiciliata and the new species should be
assigned to a separate genus.
Allerastria R. M. Brown, new genus
Type species: Yrias albiciliatus Smith, 1903
Adult. Head with eyes of both sexes large, round, greater in diameter than
width of front; front (fig. 2, 4) with a rounded projection, scaling giving front a
squared appearance when viewed laterally; labial palpi upturned, second
segment nearly straight, paralleling front, third segment short, conical to
middle of eye; antennae serrate in both sexes, males with ventral setae much
25(2): 136-145, 1986(87)
137
longer than in female, nearly equal to diameter of antennal shaft; male
antennae with 50-57 segments, female 48-53 segments. Thorax robust, fore
tibia with epiphysis arising approximately one-third distance from basal end of
tibia in both sexes; epiphysis shorter in females; metathoracic tibia of males
slightly swollen with long hair scales on the inner surface forming a vestigial
hair pencil, both pair of spurs present. Abdomen slender in males, more robust
in females, extending beyond hind wings, abdomen without dorsal tufts.
Fore wings longer than wide, apex angulate, outer margin rounded; Sc free,
ending seven-tenths from base; Ri from discal cell; R3 anastomising with R4
forming an accessory cell; R2 from top of accessory cell; R5 from apex of
accessory cell; Mx from bottom of accessory cell widely separated from M2 and
M3; end of discal cell open; M2 and M3 from lower angle of discal cell, M3 closer
to M2 than to CuAL; CuA2 arising from beyond middle of cell; 1A straight and
free. Hind wing full and without angulation; Sc and R confluent for one-fourth
of length of cell; R and Mx separate from upper angle of cell; M2 and M3 from
lower angle of cell, M3 closer to CuAi than to M2; M3 and CuAx occasionally
stalked; CuA2 arising from middle of cell; cell open; 1A and 2A straight and
free.
Male genitalia (fig. 1, 3). Valvae simple long, slender with parallel sides,
length 6—7 times width; inner surface of valvae moderately setose; uncus long,
tubular, down hooked, with lateral setae; scaphium long, slender, stalk with a
widely bifurcated tip, area between tips roundly concave, scaphium length
.55— .65 mm; juxta with basal margin deeply excavated; saccus, variable;
aedaeagus 1.0- 1.3 mm long, .25 -.33 mm wide.
Female genitalia (figs. 5, 6). Corpus bursae round to oval, membranous,
without signum; ductus bursae membranous, short; ostium with sclerotized
collar; posterior apophyses shorter than anterior apophyses, length 0.4-0. 5
mm to 0.75-0.8 mm; ovipositor lobes well developed, 0.7 -0.8 mm in length,
densely covered with setae.
Diagnosis. The species of Allerastria can be separated from those of Cobu-
batha Walker (1863) by a number of characters. In both sexes of Allerastria the
front is projecting greatly beyond the eyes, but less so than in the genus
Amiana Dyar (1904). The third segment of the labial palpi in Allerastria are
short and conical, slightly longer than their diameter, where as in Cobubatha
the length of the third segment is at least twice the diameter. The male
antenna has the ventral setae much longer than in Cobubatha. The species of
Allerastria, similar in color and maculation, have the median areas of the fore
wings predominantly cream- white and differ from much of the Cobubatha
species which have a dark brown median band on the fore wing. The male
genitalia of Allerastria have the valvae long, narrow with parallel sides, in
Cobubatha these structures broaden toward the apex and are not quite so long.
Distribution. Allerastria flies in the deserts of the southwestern United
States, and the San Joaquin Valley, California. The majority of specimens
used in this study are from southern California. The moths are on the wing
from April through September.
Etymology. Allerastria is to read as another (alios) erastria and is feminine.
138
J. Res. Lepid.
Figs. 1-2, Male genitalia. Allerastria albiciliata. la main body of genitalia;
1b aedaeagus; 1c degrees of uncus downflex. 2a head, left
lateral; 2b front.
Figs. 3-4, Male genitalia. Allerastria annae. 3a main body of genitalia; 3b
aedaeagus; 3c degrees of uncus downflex. 4a head, left lateral;
4b front.
Figs. 5-6, Female genitalia. Fig. 5 Allerastria albiciliata. Fig. 6 A. annae.
25(2): 136-145, 1986(87)
139
Fig. 7-14, Adults. Fig. 7 Allerastria albiciliata albiciliata, male. Fig. 8 A. a.
albiciliata, female. Fig. 9/4. a. pau/a, male, Holotype. Fig. 10/4. a.
paula, female. Allotype. Fig. 11 A. a. chacoensis, male, Holotype.
Fig. 12/4. a. chacoensis, female, Allotype. Fig. 13/4. annae, male,
Holotype. Fig. 14 A. annae, female, Allotype. Illustration
2 x natural size.
140
J. Res. Lepid.
Key to Species,
BASED ON MACULATION
la) Underside wings prominently bicolored, basal half cream-white to
white, distal half lead-gray to tan . 2a.
lb) Underside wings not as in la, uniformly colored cream-white .
. annae n. sp.
2a) Small, fore wing length 9.0—10.0 mm, heavly suffused with
brown scaling, from the San Joaquin Valley (Tulare Co.),
California . albiciliata paula n. subsp.
2b) Larger, fore wing length 9.0-13.0 mm, from the southwestern
(Arizona, Southern California, Nevada, and New Mexico) United
States. Upper side fore wing white, tan or pink . 3a.
3a) Upper fore wing (length 9.0—11.0 mm) may or may not have a
pink flush. Upper fore wing crossed with basal sub-terminal lines
lead-gray. Median area varies from white to pink. Southern
California, western Arizona and Nevada .
. albiciliata albiciliata.
3b) Upper fore wing (length 11.0-13.0 mm) cream-white to tan with
light brown scales scattered over wing. In well marked specimens
brown scaling forms indistinct cross lines. No lead-gray color or
contrasting median area as in 3a. Northwest New Mexico .
. albiciliata chacoensis n. subsp.
BASED ON MALE GENITALIA
la) Uncus down flexed approximately 163° (fig. lc) with heavy setae
laterally arranged; juxta basal margin deeply excavated to near
caudal margin (fig. la) . albiciliata.
lb) Uncus down flexed approximately 50° (fig. 3c) with fine setae
laterally arranged; juxta with basal margine deeply excavated to
caudal margin (fig. 3a) . annae n. sp.
BASED ON FEMALE GENITALIA
la) Ductus bursae nearly twice as long as wide; corpus bursae
regularly oval; ductus seminalis rapidly narrows to straight tube
leading to the right . albiciliata.
lb) Ductus bursae short, wider than long; corpus bursae irregularly
round with right caudal quadrent roundly projecting, ductus
seminalis broadly based and tapers to a spiraled tube leading to
the right . annae.
Allerastria albiciliata albiciliata (Smith) new combination
(figs. 1, 2, 5, 7, 8)
Yrias albiciliatus Smith, 1903, Trans. Amer. Entomol. Soc. 29:215-216. (TL:
Yuma Co., Arizona)
25(2): 136-145, 1986(87)
141
Eustrotia bifasciata Barnes & McDunnough, 1912, Canad. Entomol., 44:218.
(TL: La Puerta Valley, San Diego Co., California)
Nerastria albiciliatus, McDunnough, 1938, Check list of Lepid. of Canada and
U. S. Amer. Part 1, Macrolepidoptera, Mem. So. Calif. Acad Sci., 108.
Cobubatha albiciliata, Franclemont & Todd, in R. W. Hodges et al., 1983,
Check List of the Lepidoptera of America North of Mexico, p. 132.
The description of albiciliata by John B. Smith and the description of Eustro¬
tia bifasciata by Barnes and McDunnough are sufficient to make further
descriptions of maculation unnecessary. However, the genitalia of either sex
has not been described.
Male genitalia (fig. 1). Valvae long, narrow, with slight constriction midway
between base and apex, costa with long setae, apex rounded and clothed with
long setae, sacculus and median ridge with short setae; saccus tapering to a
blunt point; uncus (fig. lc) sharply down-flexed with apical half slightly
swollen, terminating in a sharp spine, long prominent setae laterally arranged;
scaphium with apex widely bifercated, slightly concave between tips, narrow¬
ing to a long thin shaft to point of attachment; juxta with sides incurved, basal
margin deeply excavated nearly dividing juxta in two, caudal margin straight;
aedaeagus (fig. lb) robust, armed with flat, narrow chitinous structure.
Female genitalia (fig. 5). Corpus bursae oval, without signum or other
structures; ductus bursae membranous; ostium with narrow, lightly chitinized
band at caudal opening of ductus bursae; bursae seminalis arising ventrally
from moderately broad base, narrowing rapidly to a straight tube; posterior
apophyses 0.5 mm long, anterior apophyses 1.0 mm long; ovipositor lobes well
developed and densely covered with setae.
Distribution. Arizona: Coconino Co.; Maricopa Co.; Pima Co.; Santa Cruz
Co.; Yuma Co. California: Imperial Co.; Inyo Co.; Kern Co.; Mohave Co.;
Riverside Co.; San Bernardino Co.; San Diego Co. Nevada: Clark Co.
Remarks. Two hundred forty seven specimens (78 males and 169 females),
6 genitalic and 3 wing slides have been studied.
Allerastria albiciliata paula R. M. Brown new subspecies
(figs. 9, 10)
Male. Head cream-white with scattered gray-tan scales; antennae tan and
gray checked. Thorax ventrally cream, dorsally cream with scattered gray
scales; prothoracic tibia gray with middorsal cream-white spots, scales over
epiphysis cream- white; tarsi gray with cream- white at joints; mesothoracic leg
with longest spur 2.5 times longer than shorter; tibia dorsally gray with tufted
middorsal cream- white scales; tarsi gray with cream-white at joints; metathor-
acic leg with two pair of spurs, longest upper spur 2.0— 2.5 times longer than
shorter; tibia cream- white with very little gray; tarsi light gray, cream- white at
joints. Abdomen ventrally cream-white, dorsally gray with cream-white bands.
Fore wing above with basal area cream- white with heavy overlay of gray
scales; t.a. line sinuous, tan with basal border heavy gray, distal border less
defined by gray scales; median area light tan, median band represented by a
gray square on costa; t. p. line light gray, lightly outlined by dark gray scales,
with white scales on the veins; subterminal area light tan; fringe with spatu-
late scales of various length, concolorous with subterminal area; fore wing
142
J. Res. Lepid.
below shiny with inner half cream- white, outer half gray- white. Hind wing
above, shiny, with inner half cream- white, outer half gray; below marked as
above but with more color contrast. Fore wing length 9.0-10.0 mm.
Female. Slightly larger than male, with maculation the same.
Genitalia. As in nominate subspecies.
Types. Holotype, male, California (Tulare County), Exeter, 7 -VI-1924, (R.
M. B. slide #309). Allotype, female, California, (Tulare County), Exeter,
15-VI-? (R. M. B. slide #324). Paratypes, 3 males, same locality as types, data
as follows; 5-IX-1924, R. Dodge; 18-VII-1924, R. Dodge; 15-VI-1940, E. A.
Dodge. The types and paratypes are in the collection of the California Academy
of Sciences, San Francisco, California.
Distribution. This moth is known only from the type locality and is on the
wing from June to early September.
Remarks. Five specimens (4 males and 1 female), 4 genitalic slides and 1 slide
of the wings have been studied.
Subsequent to the photograph (fig. 10) of the allotype, an Anthrenus sp.
(Coleoptera: Dermestidae) devoured the thorax leaving only the head, legs and
wings. These parts have been attached to paper supports and are still useable
for identification. The abdomen is mounted on a slide as noted above.
No difficulty should be encountered in recognizing this subspecies; paula is the
smallest and darkest taxon in this genus. The heavy brown overlay gives this
moth a distinctive appearance.
Etymology. I am calling this moth paula because of its small size. The name
is feminine.
Allerastria albiciliata chacoensis R. M. Brown new subspecies
(figs. 11, 12)
Male. Head cream- white with tan scales; antennae checked with tan; thorax
cream- white, dor sally scattered with tan scales; prothoracic leg, tibia dor sally
gray with cream-white band midlaterally, scales over epiphysis cream-white;
tarsi gray with cream-white at joints; mesothoracic leg with longer spur 2.0
times longer than shorter spur; tibia dorsally scattered with gray scales, with
middorsal cream-white tufted scales; tarsi gray with cream-white at joints;
metathoracic leg with two pair spurs, longest spur 2.3 -2.5 times longer than
shorter spur; tibia cream- white with very little gray; tarsi dorsally gray with
cream-white at joints; abdomen ventrally cream- white, dorsally with faint tan
bands. Fore wing above, all lines weakly represented, ground color cream-
white with mixture of light and dark tan scales; costa with seven variable
dark-tan checks; basal and t. a. lines variably present; subterminal area with
heaviest concentration of dark-tan scales; subterminal line present and scal¬
loped. Fringe cream-white with long spatulate scales, dark-tan checks at end of
veins. Fore wing below, shiny with inner half cream- white, outer half tan. Hind
wing below marked as fore wing below. Fore wing length 11 — 13 mm (Holotype,
11 mm).
Female. Simular in size and color with maculation less distinct than in male.
Genitalia. As in nominate subspecies.
Types. Holotype, male, New Mexico, San Juan County, Chaco Canyon
25(2): 136-145, 1986(87)
143
National Monument, 2-VIII-1962, S. F. Wood. Allotype, female, New Mexico,
San Juan County, Chaco Canyon National Monument, 3-VIII-1962, S. F.
Wood, Paratypes, 3 males and 5 females. Same locality and collector as types,
data as follows; lcf 8-VII-1962; lcf 1? 17-VII-1962; lcf 2$ 2-VII-1962; 1$
3 -VIII- 1962; 1$ 6 -VIII- 1962. The types and paratypes are in the collection of
the Los Angeles County Museum of Natural History, Los Angeles, California.
Distribution. This moth is only known from the type locality. It is on the
wing in July and August.
Remarks. Ten specimens (4 males and 6 females), and two genitalic slides
have been examined.
This moth can be seperated from the other subspecies by the general distribu¬
tion of tan scales and extremely weak markings. The maculation of the fore
wing is not divided into easly recognizable areas, although the tan scaling
forms weak striations.
Entymology. I have named this moth after the Chaco Canyon National
Monument to honor and point out the valuable role the national park system
plays in preservation of the wildlife resource. For with out this great system
and the many dedicated people the rare and unusual would have been lost long
ago.
Allerastria annae R. M. Brown new species
(Figs. 3, 4, 6, 13, 14)
Male. Head (fig. 4) dirty cream-white; labial palpi upturned to above middle
of eye with scattered lead-gray scales; antennae, lead-gray with white checks.
Thorax dirty white with light pink tinge; collar and tegulae with most pink;
prothoracic leg cream-white, tarsus lead-gray with white at joints, epiphysis
three-fourths fore tibial length; mesothoracic leg marked as prothoracic leg;
metathoracic leg marked as previous legs. Above fore wing with basal space
bicolored, inner area concolorous with thorax, outer lead-gray; costal area
above discal cell with two diffused white spots; t. a. line sinuous, lead-gray,
basally edged with a few white scales, distally by rust-red; t. p. line lead-gray,
basally shaded red, distally with lighter gray, t. a. line begins on costa, crosses
to vein CuA1? accompanied by scattering of white scales forming a faint line,
thence basad to median shade, turning then to inner margin; median area light
gray-tan, divided in costal area by median shade. Subterminal line represented
by white scales on veins, subterminal area tan with darker lunuals at vein
ends. Fringe gray. Hind wing ground color concolorous to thorax, distal half
with light gray shading. Fringe concolorous with thorax. Wings below un¬
marked, concolorous with thorax. Fringe on fore wing slightly darker than on
hind wing.
Female, similar to male in maculation, the markings less contrasting.
Male genitalia (fig. 3). Valvae long, narrow with parallel sides; apex rounded,
heavily clothed with setae on distal half, basally naked except for a small
cluster of setae on low median ridge; saccus base square and one-third saccal
width; uncus (fig. 3c) tubular, long, pointed, down-flexed, short fine setae
laterally arranged; scaphium with apex widely bifurcated, deeply concave,
narrowing to a long narrow shaft; juxta bifid, deeply excavated basally and
apically appearing as two triangular units narrowly united; aedaeagus (fig. 3b)
144
J. Res. Lepid.
robust, less than combined length of tegumen and saccus, without internal
armature or spicules, posterior end produced into a shelf-like projection, dorsal
surface heavily chitinized with short stout setae. Length three times diameter.
Female genitalia (fig. 6). Corpus bursae irregularly oval with a membranous
projection on right caudal quadrent; ductus bursae short and asymmetrically
placed; ostium with narrow chitenized band separated from caudal opening of
ductus bursae; ductus seminalis arising ventrally from a very broad base and
narrows to a spiraling tube. Apophyses short, not reaching ostium; ovipositor
lobes well developed and densely covered with setae.
Fore wing length in holotype, 13.5 mm; allotype 13.0 mm; paratypes, 12-13
mm.
Types. Holotype, male and Allotype, female, California, Inyo County, Death
Valley National Monument, western mouth Titus Canyon, elevation 1000 ft.
(305 M), 6-IV-1977, Richard M. and Paula J. Brown. The genitalia of the
holotype is mounted on R. M. B. slide #302, and the allotype is on R. M. B. slide
#318. Paratypes, 2 males, 7 females, same locality and data as holotype.
California: Inyo County; 1$ Furnace Creek Death Valley, 10-IV-1931, G.
Willett; 1$ Triangle Springs Death Valley, 11-12-IV-1942, G. Willett; 1$
Mesquite Springs Death Valley, 19-22— IV-1943, G. Willett; Riverside County;
lcf Palm Springs, 21-IV-1920; San Bernardino County; 1§ Baldy Mesa,
9-IV-1932, J. A. Comstock; 12 near Barstow, 10-V-1940, C. Ingham; lcf
Yermo, 28-VI-1938; lcf Yermo, 7-IV-1939. The National History Museum of
Los Angeles County, California will receive eight paratypes, one pair of
paratypes to the National Museum of Natural History, Washington, D.C. The
balance of the type material will be in the collection of the California Academy
of Sciences, San Francisco.
Distribution. The desert regions of southern California. As more specimens
are taken, it probably will be found to fly sympatrically with A. a. albiciliata.
On the wing from April through June.
Remarks. Twenty two specimens (6 males and 16 females) and 8 slides of the
genitalia were studied. This is an extremly variable species in maculation. It
varies from nearly immaculate individuals to those like the well marked
holotype. The first color to be lost is the rust red, the lead-gray band then fades
but never completely disappears. Allerastria annae is very close to albiciliata in
maculation but lacks the sharp definition of pattern found in albiciliata.
Allerastria annae also has much less contrast between the light and dark areas
of the hind wing than is found in albiciliata.
The male genitalia of annae can be told from those of albiciliata by the uncus
being down flexed approximately 50° (fig. 3c) . In albiciliata the scaphium has a
long shaft with parallel sides, whereas in annae the sides gradually diverge to a
widely bifurcated apex. Also annae can be separated from albiciliata by the
deep basal excavation of the juxta found in annae which gives an appearance of
two triangular units losely united.
Etymology. This moth is named after my wife, Ann, who has given so much
in support and understanding. The name is feminine.
Acknowledgments. Special thanks to Robert W. Poole, National Museum of
Natural History, for reviewing my specimens and the original manuscript, his
confirmation of my conclusions and critical comments are greatly appreciated. I
25(2): 136-145, 1986(87)
145
am also indebted to Julian P. Donahue, National History Museum of Los
Angeles, and to Paul H. Arnaud, Jr., The California Academy of Sciences, for
without their generous loans of specimens this paper would have been much
less comprehensive. Thanks to my wife, Ann, who produced the photographs
used in this paper, and also to two anonymous reviewers who caused a great
deal of work.
Literature Cited
BARNES, WM. & J. MCDUNNOUGH 1912. New Noctuid Species. Canadian Entomol.
44:216-218.
DYAR, HARRISON G. 1904. Additions to the List of North American Lepidoptera,
No. 2. Proc. Entomol. Soc. Wash. 6:103—117. (Orig. descrip of Amiana on p.
104)
FRANCLEMONT, JOHN G. & E. L. TODD IN RONALD W. HODGES, ETAL. 1983. Check List
of the Lepidoptera of America North of Mexico, p. 132.
MCDUNNOUGH, J. 1937. Notes on North American Noctuid Genera. Canad.
Entomol. 69:40-47, 58-66. (Orig. descrip, of Nerastria on p. 65.)
- 1938. Check List of the Lepidoptera of Canada and the United States of
America, Part 1, Macrolepidoptera. Mem. So. Calif. Acad. Sci., 1:108.
SMITH, JOHN B. 1903. New Noctuids for 1903, No. 4, with notes on certain
described species. Trans. Amer. Entomol. Soc. 29:191-224, Plate III.
Journal of Research on the Lepidoptera
25(2): 146-148, 1986(87)
Observations on Problems, bulenta
George O. Krizek
2111 Bancroft Place, N.W., Washington, D.C. 20008
Paul A. Opler
5100 Greenview Ct, Fort Collins, CO 80525
The rare skipper, Problema bulenta (Boisduval and LeConte), is
uncommonly observed and has never been photographed in nature.
Here we report behavioral and flower use observations made in July,
1984 at Blackwater National Wildlife Refuge, Dorchester County,
Maryland.
Previous nectar utilization has been reported by Jones (1926), who
observed the species visiting pickerelweed (. Pontederia cordata ) in
North Carolina and by Covell and Straley (1973), who reported bulenta
visiting swamp milkweed ( Asclepias incarnata) in Virginia. At the
Maryland locality P. bulenta was fairly abundant and was observed by
several persons, and as a result, more flower visiting observations were
possible. The primary nectar source at Blackwater NWR was button-
bush ( Cephalanthus occidentalis) . Secondary nectar sources observed
were the two previously reported, swamp milkweed and pickerelweed,
as well as red clover ( Trifolium pratense ) and dogbane ( Apocynum
cannabinum) (J. Fales, W. Grooms, R. Smith, pers. comm.).
In 1984, adults were seen from June 20 to July 14 — being most
common later in the flight period. Our observations and those of J.
Fales indicate that females are seldom seen at flowers and vary from 4
to 10 males seen for every female. Females may spend more time in the
immediate vicinity of their host — suspected to be a large grass. Adults
fly very close to the water at all times; most were seen within 30 cm.
The highest above water was one seen 1.5 m. The flight is rapid, strong
and noisy. Individuals seem to return again and again to the same area
of a nectar plant. When visiting buttonbush these skipper usually visit
low flowers preferring to rest on the under surface of the inflorescence,
a site that is often in shadow. At the Maryland locality the wind blows
almost constantly in variable gusts. The butterflies at flowers are
constantly turning and moving from flower to flower. Flower visitation
is from 10.00 to 15.00 hr; after that time the butterflies are no longer to
be found.
Other butterflies sharing the buttonbush flowers with P. bulenta were
Epargyreus clarus, Erynnis horatius, Ancyloxipha numitor, Wallengre-
nia egeremet, Poanes viator (abundant), Phyciodes tharos, and Vanessa
virginiensis.
25(2): 146-148, 1986(87)
147
This skipper is very difficult to photograph. One must go into the
river’s water or stand at its muddy edge. This together with the almost
constant wind, and the low, nervous flight of the insect makes such
attempts trying at best.
The habitat is similar to that found along the Chickahominy River in
Virginia (Coveil and Straley, 1973). It seems likely the Maryland
colony is univoltine as suggested by Opler and Krizek (1984). Further
investigation is necessary to reveal the host plant and reproductive
biology of this uncommon insect.
Acknowledgements. We thank John H. Fales, Calvert, Maryland; Richard
Smith, Baltimore; and William C. Grooms, Tysons Corner, Virginia, for sharing
their field notes on this butterfly.
Literature Cited
COVELL, C. V., JR. & G. B. STRALEY. 1973. Notes on Virginia butterflies, with two
new state records. J. Lepid. Soc. 27: 144-154.
JONES, F. M. 1926. The rediscovery of Hesperia bulenta Bdv. and LeC., with
notes on other species (Lepidoptera: Hesperiidae). Ent. News 37: 194-198.
OPLER, P. A. & KRIZEK, G. O. 1984. Butterflies east of the Great Plains: an
illustrated natural history. Johns Hopkins University Press, Baltimore.
xvii+294 pp.
148
J. Res. Lepid.
Figures 1-2. Adult Problems bu/enta nectaring at buttonbush {Cephalan-
thus occidenta/is) at Blackwater National Wildlife Refuge,
Dorchester County, Maryland, on July 14, 1984.
1. Male, 2. Male.
J. Res. Lepid.
149
Book Reviews
THE BIOLOGY OF BUTTERFLIES. Symposium of the Royal Entomological
Society of London, Number 11 (R. I. Vane-Wright and P. A. Ackery, Eds.).
Academic Press, London, 1984.
Purchase the book if you take your lepidopterology at all seriously. That
addresses the overall picture quite sufficiently. Of course, the thing is most
certainly not without its peculiar flaws, although in fairness this review often
deals with shortcomings inevitable in any such tome covering comparably
broad terrain.
The butterfly symposium itself took place in September 1981 at the British
Museum of Natural History, coincident with the eightieth year of Prof. E. B.
Ford, in whose honor the event was dedicated. A star-studded cast of 44 signed
off on the 33 articles ultimately shepherded to press by the capable hands of
Vane-Wright and Ackery. The articles are organized into eight major areas of
research on butterfly biology, which here seem most sensibly grappled with in
the order in which they appear.
I. Systematics. Since this is a volume on butterfly biology, it is not surprising
that butterfly taxonomy is allotted only minimal page space. Indeed, Ackery
sequesters such considerations in but the first 13 pages of the total 429, with a
healthy chunk of that devoted to recounting and judging faunistic works of the
world. All in all, we hear relatively little about butterfly faunistics as compared
to butterfly taxonomy (and, of course, bloated and imbalanced work on limited
faunas seems to be the relentless vogue in the latter). Not so with Ackery’s
concise and bibliographic faunistic summaries — hats off to him for skipping
the pedestrian, and pointing the way into an important yet often neglected
literature.
II. Populations and Communities. This section contains two lengthy and two
very brief articles. An Ehrlichian overview of population structure sensu strictu
is both expected and appropriate in a volume of this stature, since the Stanford
studies are among the forerunners. I’ve read essentially everything the Ehrlich
group has put out over the years, and this is one of the most readable and
widely appealing of their available reviews. More is known about population
structure in Euphydryas than in most other species, and it is sobering indeed to
hear Ehrlich berate his favorite creatures, and call for studies on a less biased
taxonomic sampler of butterflies.
Gilbert then expands the focus to entire butterfly communities; given
Ehrlich’s caution, it is no surprise that generalizations are even fewer here. In
short, the number of possible explanations for observed patterns increases
explosively as one moves from single to multiple-species studies (infrataxono-
mic differences even notwithstanding). As a synopsis of this still nascent field
Gilbert’s article is fine. A gem within it is the paraphrasing of Munroe, who in
his thesis had written the kernel of island biogeography well before it was
popularized by MacArthur & Wilson’s subsequent monograph. However, Gil¬
bert quotes Munroe to establish a sad point, namely that “the slow progress of
butterfly ecology [is because! ... it has often been an afterthought of systema¬
tic or genetic studies.”
150
J. Res. Lepid.
The final two short articles in this section do not belong. Pollard’s simply
doesn’t begin to do justice to the important field he has helped to engineer. Read
his journal articles on relative abundance instead, and the terminal paper in
the symposium volume. Morton’s asks how the process of marking butterflies
influences their subsequent activity. While there has never been much doubt
that mark effects occur commonly, there are also few published studies addres¬
sing the issue. Morton’s paper is generally helpful in this latter regard, but his
data are useful only insofar as one tolerates the failure to measure catchability
differences, and other factors central to analysis of recapture probabilities (see
below).
III. The Food of Butterflies. This third section mirrors its predecessor in
having two long and two short articles. Chew & Robbins lead off with one of the
long ones, on egg-laying in butterflies. Their article embraces a large literature,
hitting subtopics as diverse as oogenesis, selecting oviposition sites, and the
evolution of oviposition specificity. Give them an ‘E’ for effort. It is partly the
magnitude of their selected topic (too broad for one article), but mostly their
choppy prose and superabundant citations which run the article aground.
Large segments of the text are choked with 2-3 times as many references as
necessary, and accordingly this is one of the more difficult to read among the
symposium articles. Scan through it for the goodies to your liking. Their final
section is probably the most provocative, and ushers in the notion of ‘large-scale
evolutionary jumps,’ a subject taken up independently in other contexts by
other authors in the volume.
Singer, whose writing is vastly clearer, addresses a restricted but closely
related array of topics. He first reviews host discrimination by females, and
then turns to the consequences of female choice upon (the essentially ship¬
wrecked) larvae. A trademark of Singer’s is careful scrutiny of intervening
variables — what might loosely be described as the dozen or so factors you
couldn’t measure, but which your critics seize upon with glee. His trademark is
evident throughout the latter half of this article (e.g., pages 85-87). It makes
for tempered discussion, and, consequently, good reading.
At the end of this chapter are two more brief articles. Courtney’s is scarcely a
page, is merely a listing of homilies about habitat and footplant selection, and
again does not belong in the volume. My advice is the same as for Pollard’s
effort in Chapter II: go read Courtney’s fine original research papers instead.
Edgar’s short data paper marshalls believable evidence that plants in the
family Parsonsiae represent ancestral foods for danaines and heliconiines.
IV. Predation, Parasitization, and Defence. This section contains a smatter¬
ing of articles dealing with threats to butterflies — who eats them, where,
when, and why, and the consequences in evolutionary time. Dempster asks the
damaging question: what in fact do we know of the natural enemies of
Lepidoptera themselves (cf. the abundant indirect evidence of their effects)?
The essential lesson from his lead article is straightforward, and can’t be
emphasized enough — we know depressingly little about the influences of
natural enemies on lepidopteran populations in the field. Lane’s tantalizing
short second article, on ectoparasitic midges on butterflies, only reaffirms
Dempster’s point (an excellent parallel treatise to Lane’s is Treat’s book on
moth mites). In sum, our understanding of predators and parasites remains in
‘seek and describe’ mode.
J. Res. Lejrid.
151
These tentative articles give ground to Brower’s methodical and exacting
dissection of lepidopteran chemical defense. The longest of the Symposium
articles, it is also among the best, a basic and refreshing subplot within it being
re-categorization of the myriad terms applied in the literature on chemical
defense and mimicry. Brower first establishes these theoretical constructs, and
then marches into the fray and sorts through the booty of published, often
fragmentary information. His differentiation between Class I (noxious) and
Class II (innocuous) defensive chemicals becomes central to arranging the
mess, and understanding the roles played by diverse assemblages of chemicals
in the overall picture of chemical defense. Brower’s attention to spatial and
temporal diversity in predator behavior is similarly welcome. As with Singer,
Brower has the keen eye for how to deal with observed variation in a systema¬
tic fashion.
Marsh et al.’s short article has the unenviable distinction of following Brow¬
er’s and preceding Turner’s. Their idea is laudable: test the anti-tumor action of
various lepidopterous extracts. But the data are few (though interesting), and
the recitations smack a little much of the narrow approach against which
Brower just finished campaigning so successfully.
Turner opts for the moderator’s stance, balancing opposing arguments while
dismantling traditional dichotomies between Batesian and Mullerian mimicry.
This he caps off with a lengthy and poignant discourse on saltational genesis of
mimicry complexes. Indeed, by the end of the article, Turner has roamed fully
into a general treatment of neo-Goldschmidtian punctuationalism (his tongue-
in-cheek “evolution by jerks”). Throughout he draws upon the exemplar
tropical heliconiine-ithomiine mimicry rings to bolster specific arguments.
Turner’s temperance helps to unravel the various concepts, and his article can
certainly stake its claim as an educated precis on mimicry.
The reader must again endure two plus pages of the suboptimal after a
masterpiece. In their introduction to the symposium, Vane-Wright et al.
indicate that Gibson’s automimicry article “generated much discussion ... at
the meeting.” Within the walls of said meeting is where this off-the-cuff model
should have stayed to ripen a bit. Field workers with an accompanying feel for
modeling will have little difficulty flagging the several tenuous assumptions
and their scant support from data. For automimicry, start with Brower et al.
(1967), et seq., and work yourself forward through the literature from there.
V. Genetic Variation and Speciation. Leading off the second half of this
volume is a variegated assembly of papers dealing with microevolutionary
matters. Brakefield’s is the principal article, a classical British ecological
genetic investigation of spotting pattern in satyrines. He devotes the first ten
pages to detailed and data-intense elaboration on the classification and herita-
bility of these demure undersurface spots, and then traverses a shopping list of
selective pressures potentially responsible for the geographic and populational
variation in spotting.
The “boundary phenomonon” is certainly among the funkier discordant
morphological patterns thrown by Maniola. The undersurface spotting regime
of this butterfly shifts abruptly along a front only dozens of meters wide in
southwestern England, and the front itself moves about in both time and space.
There is still no overpowering explanation for this pattern, despite several
decades of research. Brakefield somewhat belabors the ambivalent results with
152
J. Res. Lepid.
this and other aspects of the Maniola story, but gets on track with his own
thing — the spots as anti-predator devices, fluctuating selective pressures, and
a healthy plea for populational work on the immatures.
Brakefield’s plate of 119 ‘pressed’ Maniola on pages 174-175 is a welcome
sight. (It reminds me of the cabinets full of quite prostrate Gerould Colias who
have cohabited over the years with me in my niche in the museum). More
importantly, of course, it is just about the only visible affirmation in the
symposium that properly executed morphological work has always been and
will always continue to be central to good evolutionary study. This too often
gets billed as an antiquated tenet, in this heyday of gelled and pureed creatures
(and narrowly defined biochemical jobs in evolutionary biology, and divested
museum holdings).
Kitching picks up on the subject of chopped butterflies in the second article,
but only offers a breezy two cents’ worth on his electrophoretic work on
danaids, and the possible concordance between his data and the morpholgical
cladistic treatments of Ackery & Vane- Wright. Of what value is that? Granted,
there are concerns other than review articles when one is completing a doctoral
dissertation, but what an apparently lost opportunity for a coming lepidopterist
to publish some hot-off-the-press research in a major tome. So, why?
Gordon follows with a brief yet stimulating notion that mimicry (and possibly
speciation) in each African Acraea is linked to dispersal, which in turn is linked
to patterns of local extinction. Though he errs in the same manner as others
throughout the symposium by equating differences in recapture probability
entirely to one of its several confounding components (in this case, to dispersal),
his continued pursuit of the subject should uncover some treasures.
Pierce wraps up with another short piece, but one which strikes an appropri¬
ate balance between the data presented and the conclusions drawn. The
suggestion that lycaenids speciate more rapidly because of low deme sizes and
selection by females for both foodplants and ‘ant’ plants is most plausible. We
can also now add lycaenid larvae to the growing list of bizarre entomological
edibles.
VI. Sex and Communication. This is the most mature chapter overall in the
volume; and Silberglied’s is easily the best paper in this chapter, being both
provocative and scholarly in content and well written. Smith’s is a close second,
with the differences in approach and opinion between he and Silberglied
appearing to be in large part semantic (or reflecting ‘taxonomic scale,’ cf. the
Introduction).
Silberglied treats us first to Darwin’s view on lepidopteran coloration and an
accounting of its diversity, and then settles in on visual signals important in
male and female communication, respectively. His take-home message is that
female butterflies choose not on the basis of visible male colors, but rather on
the basis of UV signatures and smells; he leaves us thinking along intrasexual
lines for explanations of male butterfly colors.
Smith analyzes mate selection in Danaus and Hypolimnas, offering one of the
better blends of data and discussion in the volume. A main thrust of his is
distinguishing between random preferential mating, and assortative preferen¬
tial mating. It remains to be seen whether Smith’s complex findings are
generalizable throughout Lepidoptera. However, Smith takes high marks
among the 44 authors for his frequent admonishments about the inadvisable
lumping of heterogeneous sub-classes of data, and the certainty of subsequent
errors in interpretation.
J. Res. Lepid.
153
Three shorties follow. Platt et al. offer a short data paper conclusively showing
lack of differential mate selection in tiger swallowtail morphs. Vane-Wright
notes, in particular, how male narcissism might be a unifying force for
apparently equivocal and/or puzzling results in butterfly ethology. Finally,
Clarke talks a little about sex-ratio distortions in gypsy moth and Hypolimnus
broods.
The terminal paper, by Boppre, addresses the chemical aspects of communica¬
tion among butterflies. Admittedly, much of our general knowledge of this
subject comes from experiments with moths — with butterflies, it has been
largely anecdotes, some major works notwithstanding. Boppre dutifully covers
his material (androconia, pheromones, associated behavior, etc.) but in at least
twice the number of words required.
VII. Migration and Seasonal Variation. Baker’s is the primary paper in this
Chapter of only vaguely related articles, offering a glimpse into what governs
the movement of butterflies. His temporal frame of reference is substantially
longer (lifespan) than that typical of published work on butterfly movement
(days or so), and this imparts to Baker a different and healthy perspective.
Indeed, he treats topics such as direction ratios that often never surface in more
conventional mark-recapture studies, and it is encouraging to see such initial
advances in a curiously neglected field (after all, butterflies fly, and so why
don’t we know more details about their travels than we do?).
From flight we jump inexplicably into study of seasonal polyphenism, cast in
the light of genetic assimilation. Shapiro reworks a theme he has been pub¬
lishing on vigorously for a decade, though in this paper he treats us to data
from some new taxa. I agree with the editors that Shapiro’s effort is heroic
despite equivocal results; he is also a bigger man than most to confess at the
end that “if . . . [so], one need only invoke ordinary Darwinian selection to
evolve polyphenism, and neither genetic assimilation nor anything more
arcane is necessairly required.” See his Figure 27.5 if you have doubts as to the
genetic (cf. environmental) basis of polyphenism.
Chapter VII continues its schizophrenia by shifting to an illuminating short
piece by Porter on larval basking, and its probable link with efficient digestive
activity. Two more brief, descriptive polyphenism papers follow: McLeod on
Precis', and Yata et al. on Pieris (the latter being of some intrigue since it treats
polyphenism in the immature stages).
Vni. Conservation. Pyle is the acknowledged popularizer of lepidopteran
conservation worldwide, and an article from him is obligatory. Here he focuses
on the recent eruptions of Mt. St. Helens in western North America, and the
influence this literally earth-shaking event had on butterflies in the area.
Glean the more general of Pyle’s points, since the data are necessarily scanty
and inconclusive (the appropriate comparative pre-eruption lepidopteran re¬
search sadly doesn’t exist).
The second article by Parsons examines the distribution, biology, and con¬
servation problems faced by the world’s largest birdwing butterfly. While
Parsons talks about habitat loss (e.g., encroaching oil palm plantations) and
factors affecting foodplant distribution, he unfortunately didn’t give air time to
an intriguing, tested, and successful option — ‘butterfly farming.’ This novel
technique simultaneously eases commerical demand for specimens without
impacting wild populations, puts cash into the local economy, and (probably
most importantly) fosters local interest and commitment to the conservation
154
J. Res. Lepid.
ethic. Parsons’ repeated citing of internal agency documents on the matter of
butterfly farming only makes one yearn further for an expose in the more
accessible, true public record.
This brings us to the ultimate paper in the volume. And it is the denoument —
a masterly review by Thomas of lepidopteran conservation efforts in temperate
countries. I can’t praise it enough. In fact, it is pointless for me to waste your
time recapping it here, except to say that it shows pithy insight on all aspects of
complex conservation issues, including: the acquisition and analysis of data on
population changes, pinpointing the factors responsible for the observed
changes, the associated political and sociological backdrops, and how these
three avenues of inquiry are (or aren’t) translated effectively into day-to-day
conservation practice. He certainly doesn’t shy away from flagging the dismal
failures among the gamut of conservation attempts.
Thomas really does have a handle on the ‘big picture,’ and I strongly urge that
his paper be read carefully, with an eye toward integrating the lessons of the
other 32 papers into the unifying framework offered in the 33rd. It is a fitting
wrap-up indeed for this symposium — lepidopteran conservation efforts have
been gaining momentum during their formative period of the past two decades,
and stand to mature in their own right during the remainder of this century.
Commentary.
As you have gathered, the symposium articles fall broadly into two size (and
content) classes — very brief reports of narrowly defined studies, and long
review articles. The short reports are of inferior quality, and detract from the
impact of the symposium volume as a whole. Why juxtapose notes of passing
interest alongside more permanent, scholarly reviews? After all, we have
journals for the express purpose of communicating such short notes (and
journal referees to reject the bad ones).
Obviously, I don’t feel these short notes at all served the editors’ stated
intention (page 1) of amplifying or highlighting accepted dogma or difficulties.
Nevertheless, there are other factors which editors must weigh (such as
affording equal air time to all participants in joint ventures). While one may
dislike the schizophrenia imparted by the short papers, Vane-Wright and
Ackery can’t be held wholly accountable for problems inevitable when concate¬
nating as many as 33 papers. Choppiness is one such unavoidable problem.
Leaving style aside, one large matter of substance glares at me through these
several hundred pages of otherwise excellent lepidopterology. Why is it that
mark-release-recapture takes it on the chin in this volume? I see much
innuendo on supposed ‘problems with MRR,’ especially the business of marking
itself, but little concrete offered in the way of justification, let alone alternative
methodology.
It is telling that authors in this symposium make essentially no mention of
Tabashnik’s research on sulphur butterfly population structure, insofar as it
applies to the theory and practice of MRR (nor do they speak of Begon’s 1979
book). Tabashnik’s 1980 paper, published in Oecologia, is the seminal work in
recent years dealing with the partitioning of recapture probability into its
biologically distinct components. Not one author attempted to break down
recapture probability here, yet each tried to interpret recapture probabilities.
There is little excuse for continued unthinking analysis of recapture probability
as if it were a unified whole. Catchability and residence are different, they
J. Res. Lepid.
155
combine to form recapture probability, and the distinction is paramount. Age
structure is also easy to monitor (via wing wear), and it too is central, but again
few authors bothered to report it.
These are unsettling omissions. I get the impression that this pooh-poohing of
MRR is traceable in large part to the intermittent reports detailing detrimental
effects of marking (as championed in part by Morton here, and others else¬
where). Really, though, so what if marking effects exist? They’re present by
definition. This begs for tempered investigation of their impact on populational
parameters, not thoughts of rejecting MRR as the basis for measuring popula¬
tion size (the fact is that few have cared to ask critical questions in this area).
Non-marking techniques certainly have their place, but they can’t yet supplant
MRR, and doubtfully ever will.
Lawrence F. Gall, Entomology Division, Peabody Museum of Natural History,
Yale University, New Haven, CT 06511 USA
BUTTERFLIES OF EUROPE, Volume 1, Concise Bibliography of European
Butterflies, Otakar Kudrna, Editor, 1985. AULA-Verlag, Postflach 1366, D-
6200, Luisenplatz 2, Wiesbaden 1, West Germany. 447 pp. DM 248 (series
subscription price DM 216).
The Concise Bibliography is the first volume to be issued of the eight-volume
BUTTERFLIES OF EUROPE series edited by O. Kudrna. Volumes 3-6 will
discuss butterfly families, while vols. 2, 7 and 8 pertain to lepidopterology,
ecology, and conservation of European butterflies.
This initial volume consists of approximately 6000 bibliographic entries in
alphabetical order by author and relating to various aspects of European
butterflies. The entries are numbered sequentially with a few alphanumeric
citations. The volume begins with a five-page Preface and a five-page Introduc¬
tion; an eleven-page Subject Index concludes the book. The citations included
date from 1901 to 1983. References are provided to earlier bibliographies that
cover publications prior to 1900.
The editor states in the Introduction that this volume is designed “ . . . to serve
the needs of all students of butterflies of Europe ...” regardless of their
professional status. This work is not intended to be comprehensive. The
citations listed were selected from a database of over 10,000 references com¬
piled during the preparation of the series as a whole. Major taxonomic papers
are included along with citations to treatises about ecology, distribution,
conservation, etc. Full citations are provided with the use of standard abbrevia¬
tions for journal titles.
The Subject Index allows the user to locate references on the basis of family,
geographic region, genetics, anatomy, and many other classifications. It does
not, however, permit the user to locate citations by genus or species. This is
perhaps the only shortcoming of the book, and to include an index to genera
and species would have increased the size of this volume considerably.
This book is well made with clear type and English text. It should be a
valuable addition to the library of anyone interested in European butterflies.
Clifford D. Ferris, Bioengineering Program, University of Wyoming, P. O. Box
3295 University Station, Laramie, Wyoming 82071.
156
J. Res. Lepid.
THE BUTTERFLY GARDEN: Turning your Garden Window Box or Backyard
into a Beautiful Home for Butterflies.
Mathew Tekulsky. 1985. Harvard Common Press, Boston, ISBN 0916782-
69-7. Price $8.95 paperback.
This charming and broadly informative book is an excellent piece for serious
lepidopterists to give their inquiring friends. Tekulsky, a professional writer,
has written the book well, and, as a consequence of research conducted in the
course of writing, has in fact now become an amateur lepidopterist.
Works like this represent a new generation of popular entomology through
emphasis on observation and data-keeping, as opposed to the collecting mania
and deadend museum ideology of earlier days. In terms of public awareness,
such Weltanschauung should be cultivated as one’s social responsibility, in
addition to the joys of a scientific hobby. Butterflies are increasingly recognized
as indicators of a world environment that is going to hell.
The factual material is general, as it must be, since the means of augmenting
butterfly densities by gardening practise obviously differ between Los Angeles
and Brooklyn. Nevertheless, a wide and thorough set of topics is covered from
classification/life cycles, life zones, to courtship, migration, foodplants and
nectar sources, and conservation. An emphasis on notetaking is a good point,
and the bibliography and citation of resources are excellent. Bob Pyle wrote the
well done introduction.
ENTOMOLOGY OF THE CALIFORNIA CHANNEL ISLANDS: Proceedings
of the First Symposium.
Menke, A. S. and D. R. Miller. 1985. Santa Barbara Museum of Natural
History, Santa Barbara, CA 93105. 178 pp. + 8 separate maps. Price $20.
paperback.
For anyone with an interest in island biogeography, as the concept is
strictly applied to islands, the California Channel Islands are perhaps the best
surveyed such areas in the world. This volume is the latest and most complete
work to date. Of the animals censused, the Lepidoptera are the second best
known group (after Orthoptera). Jerry Powell authored the principal paper on
Lepidoptera. Although he defines the paper as a preliminary overview, it
bears reading by all interested in patterns of distribution, citing problem
areas as well as general findings plus a thorough bibliography. Larry Gall
provides a neat paper on the initial recorded incursion of Strymon melinus
onto Santa Catalina Island. The sole habitat of its close relation (sister
species?) S. avalona. The paper provides a nice but too-brief lesson in morpho¬
logical character analysis by numerical techniques of intraspecific variation
and identification of potential phenetic hybrids. Scott Miller gives the intro¬
ductory perspective. Five other papers cover Orthoptera, bees, Sphecids, mea¬
ly bugs, beetles and tiger beetles. Excellent detailed finescale maps of all
islands are given in a separate envelope. My sole criticism lies in the reproduc¬
tion of typescript. Even though very well done in this case, there is something
psychologically ephemeral about non-typeset work.
Rudolf H . T. Mattoni, 9620 Heather Road, Beverly Hills, CA 90210, USA
INSTRUCTIONS TO AUTHORS
Manuscript Format: Two copies must be submitted (xeroxed or carbon papered),
double-spaced, typed, on 8V2 x 11 inch paper with wide margins. Number all pages
consecutively and put author’s name at top right corner of each page. If your typewriter
does not have italic type, underline all words where italics are intended. Footnotes,
although discouraged, must be typed on a separate sheet. Do not hyphenate words at the
right margin. All measurements must be metric, with the exception of altitudes and
distances which should include metric equivalents in parenthesis. Time must be cited on
a 24-hour basis, standard time. Abbreviations must follow common usage. Dates should
be cited as example: 4. IV. 1979 (day-arabic numberal; month-Roman numeral; year-
arabic numeral). Numerals must be used before measurements (5mm) or otherwise up to
number ten e.g. (nine butterflies, 12 moths).
Title Page: All papers must have the title , author’s name, author’s address, and any
titular reference and institutional approval reference, all on a separate title page. A
family citation must be given in parenthesis (Lepidoptera: Hesperiidae) for referencing.
Abstracts and Short Papers: All papers exceeding two typed pages must be ac¬
companied by an abstract of no more than 300 words. An additional summary is not
required.
Name Citations and Systematic Works: The first mention of any organism should
include the full scientific name with author (not abbreviated) andyear of description. New
descriptions should conform to the format: male: female, type data, diagnosis, distribu¬
tion, discussion. There must be conformity to the current International Code of
Zoological Nomenclature. We strongly urge deposition of types in major museums, all
type depositions must be cited.
References: All citations in the text must be alphabetically listed under Literature Cited
in the format given in recent issues. Abbrevations must conform to the World List of
Scientific Periodicals. Do not underline periodicals. If four or less references are cited,
please cite in body of text not in Literature Cited.
Tables: Tables should be minimized. Where used, they should be formulated to a size
which will reduce to 4 x 6V2 inches. Each table should be prepared as a line drawing or
typed with heading and explanation on top and footnotes below. Number with Arabic
numerals. Both horizontal and vertical rules may be indicated. Complex tables may be
reproduced from typescript.
Illustrations: Color must be submitted as a transparency (i.e., slide) ONLY, the quality
of which is critical. On request, the editor will supply separate detailed instructions for
making the most suitable photographic ilustrations. Black and white photographs should
be submitted on glossy paper, and, as with line drawings, must be mounted on stiff white
cardboard. Authors must plan on illustrations for reduction to the 4 x 8V2" page.
Allowance should be made for legends beneath, unless many consecutive pages are used.
Drawings should be in India ink at least twice the final size. Include a metric scale or
calculate and state the actual magnification of each illustration as printed. Each figure
should be cited and explained as such. The term “plate” should not be used. Each
illustration should be identified as to author and title on the back, and should indicate
whether the illustration be returned.
Legends should be separately typed on pages entitled “Explanation of Figures”.
Number legends consecutively with separate paragraph for each page of illustrations. Do
not attach to illustrations. Retain original illustrations until paper finally accepted.
Review: All papers will be read by the editor(s) & submitted for formal review to two
referees. Authors are welcome to suggest reviewers, and if received, submit name &
comments of reviewers.
THE JOURNAL OF RESEARCH
ON THE LEPIDOPTERA
Volume 25 Number 2 Summer 1986(1987)
IN THIS ISSUE
Date of Publication: 21 1987
A New Species of Calisto from Hispaniola with a Review
of the Female Genitalia of Hispaniolan Congeners (Satyridae)
Kurt Johnson, Eric Quinter & David Matusik 73
Records of Prolonged Diapause in Lepidoptera
Jerry A. Powell 83
An exceptional case of paternal transmission of the dark
form female trait in the tiger swallowtail butterfly,
Papilio glaucus (Lepidoptera: Papilionidae)
J. Mark Scriber & Mark H. Evans 110
The Phene tics and Comparative Biology of Euphilotes enoptes
(Boisduval) (Lycaenidae) from the San Bernardino Mountains
Gordon F. Pratt & Greg. R. Ballmer 121
A New Genus and Species from the Southwestern United States
(Noctuidae: Acontiinae)
Richard M. Brown 136
Observations on Problema bulenta
George O. Krizek & Paul A. Opler 146
Book Reviews 149
COVER ILLUSTRATION: Reproduction of watercolor by Gordon Pratt of last (4th) instar
larva, pupa, and adult of Euphilotes enoptes mojave
THE JOURNAL
OF RESEARCH
ON THE LEPIDOPTERA
1
WmMk
. ca
s ^
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THE JOURNAL OF RESEARCH
ON THE LEPIDOPTERA
ISSN 0022 4324
Published By: The Lepidoptera Research Foundation, Inc.
c/o Santa Barbara Museum of Natural History
2559 Puesta Del Sol Road
Santa Barbara, California 93105
Founder: William Hovanitz
Editorial Staff: Rudolf H. T. Mattoni, Editor
Lorraine L. Rothman, Managing Editor
Scott E. Miller, Assistant Editor
Associate Editors: Emilio Balletto, Italy
Miguel R. Gomez Bustillo, Spain "I"
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Hansjuerg Geiger, Switzerland
Otakar Kudrna, Germany
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Arthur Shapiro, U.S.A.
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THE JOURNAL OF RESEARCH ON THE LEPIDOPTERA is published four times a year, Spring, Summer,
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Mattoni at the above Beverly Hills address. The Secretary-Treasurer is Barbara Jean Hovanitz at the general
business office. All matters pertaining to membership, dues, and subscriptions should be addressed to her,
including inquiry concerning mailing, missing issues, and change of address. The owner is THE LEPIDOP¬
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of California in 1965. The President is R. H. T. Mattoni, the Vice President is John Emmel, the Secretary-
Treasurer is Barbara Jean Hovanitz. The Board of Directors is comprised of Barbara Jean Hovanitz, Lorraine
L. Rothman, and R. H. T. Mattoni. There are no bond holders, mortgages, or other security holders.
Journal of Research on the Lepidoptera
25(3): 157-178, 1986(87)
Distribution and Abundance of Butterflies in the
Urbanization Zones of Porto Alegre, Brazil
Alexandre Ruszczyk
Av. Azenha N° 330 ap. 11, Porto Alegre 90.060, RS, Brasil
Abstract The distribution of butterflies in the urban area of Porto
Alegre was analysed by means of transects of avenues and data
collected over a grid of 111 observation points. Maps were drawn
showing the urbanization zones of the city, percent of vegetation cover
as well as the distribution of 29 butterfly species. Three zones with
relative uniformity can be identified along the urbanization gradient:
B (buildings higher than four stories), vegetation cover below 20%; HB
(houses and buildings of less than four stories), vegetation cover
between 20 and 40% and H (houses, also including open areas within
the city), vegetation cover above 40%. The distribution of butterflies in
the city showed a life zone pattern very well correlated and oriented
with the urbanization gradient. The border between zones H and HB
represented a barrier for several species strongly associated with
woods or natural fields, representing the most important transition
area in the city fauna. The increase in the urbanization and pollution
was accompanied by a decrease in the number of species and indi¬
viduals registered as well as by a homogenization in butterfly distribu¬
tion. In terms of abundance and distribution of its individual elements,
the butterfly community of Porto Alegre is consistently structured in
accord with the urbanization gradient, represented as distance from
the center of the city. The predominance of this parameter is probably
due to the fact that this distance is the main conditioner of many
variables which are important for butterflies (such as urban climate,
percent vegetation cover, air pollution and human density). Species of
open areas, with high vagility, nectar feeders and with larvae feeding
on exotic cultivated plants are dominant in the city.
Introduction
Among the more esthetically pleasing animals which inhabit urban
ecosystems along with man, birds and butterflies have high ranking.
Few authors have attempted to investigate the determinants of but¬
terfly occurrence and non-occurrence in man-made environments; most
publications about butterflies in urban areas simply report a list of
species found in a given city. In a more in-depth study, Shapiro &
Shapiro (1973) studied the Staten Island (USA) butterfly community
and called attention to its homogeneity. The butterflies found in aban¬
doned lots, always the same, were increasing in number and distribu¬
tion while the native and specialized forms were declining. The first
158
J.Res.Lepid.
i
group included vagile colonizers with a high reproductive rate, feeding
on weeds and probably tolerant of air pollution. Yamamoto (1977)
studied the butterflies of Sapporo (Japan) and found that most of the
individuals belonged to a small number of species; a decline in the
butterfly fauna paralleled the increase of urbanization. Species of open
areas, which hibernate during the pupal stage and reproduce three or
more generations per year, were those more resistant to urbanization.
His results showed the substitution of forest species by open area
species. Singer & Gilbert (1978) offered some general theoretical con¬
siderations about butterfly ecology in urban environments.
Iq this work the entire urban area of Porto Alegre (Rio Grande do Sul,
Brazil) was sampled for butterflies. The main objectives were to investi¬
gate butterfly distribution over the urbanization gradient and the
influence of habitat variables on butterfly abundance.
Study Area
The city of Porto Alegre is located in southern Brazil (30°02' S, 51°14'
W), with a population of over a million inhabitants. The altitude varies
from 4 to 300 m above sea level (mean about 80—100 m). The region
has a temperate-subtropical climate with high humidity and moderate¬
ly high temperatures in the summer. The annual mean temperature is
13.8°C and the average rainfall 1322 mm.
The city is surrounded by agrarian ecosystems to the north, south and
east; to the west are found the aquatic ecosystems of Guaiba River
(Figure la). Within the city are found only remnants of woods in
hard-to-reach places in the southern sector, where urbanization has
been partially stopped. A field vegetation, either managed or aban¬
doned, presently predominates on the periphery of the city.
Over a 1:20.000 city map was laid a 5-cm grid (equal to 1 km2 real
size). Using the geometric center of each square, 111 circles 3 cm in
diameter (300 m radius or 0.283 km2 real size) were defined. The circles
corresponded to sampling subunits called observation points (OP). The
distance of each OP from OP E5 (Figure 2) in the center of the tall
building zone was considered “distance from the center of the city”. The
mean altitude of each OP was estimated as the arithmetic mean
between its highest and lowest points. Over a 1:8.000 photograph of
each OP was laid a 6 x 6 cm square of millimetered paper (0.2304 km2
actual area). The parts covered by plants, including native vegetation
as well as lawns, back yards, vacant lots and street trees, were shaded.
The calculated percentage of vegetation cover of each OP was extrapo¬
lated to the area of 1 km2 (Figure lb).
By examination of 1:20.000 aerial photographs of the city with the aid
of a stereoscope, three zones of different intensities of urbanization
could be drawn over a political map at the same scale: high (buildings
zone or zone B; vegetation cover below 20%; zero to 2 km distant from
25(3): 157-178, 1986(87)
159
the center of the city), medium (houses and buildings zone or zone HB;
vegetation cover between 20 and 40%; 2 to 7 km distant from the center
of the city) and low (houses zone or zone H; vegetation cover above 40%;
4 to 12 km distant from the center of the city). The borders of the zones
were adjusted by examination in loco. The final map (Figure lc) was
simplified to polygons, by drawing tangential lines to the borders of the
different zones of urbanization (Figure Id).
The radial arrangement of the main avenues of Porto Alegre has
determined an urbanization gradient also radial and relatively similar
in all directions from the center of the city. Over the urbanization
gradient is found a complementary gradient of vegetation covering,
also with a radial aspect and similar preferential orientation
(northeast-southeast) (Figure lb).
Zone B and industrial and shopping areas generally show less than
20% plant cover. Zone HB has under 40% plant cover, showing a close
spatial relationship with the 15-30% class in Figure lb. Zone H has in
general plant cover value over 40%, reaching a maximum of 78%. The
mean value was 39.3% (s = 17.2). The minimum value for this variable
was 7.2% in OP E4.
Methods
The distribution of butterflies was investigated using two methods:
transects, and data recording in observation points.
Transects
Four transect routes were used (AB, CD, EF and GH), along the main
avenues out from the center of the city. The censuses began at 10 a.m.
at the inner end of each route, and consisted of a round trip to the outer
end and back. Ten such censuses were done along each route. All
butterflies seen by naked eye were registered, whether flying or sitting
up to 10 meters back from the street side of the buildings. The location
of each individual was determined in relation to the nearest cross
street.
Data Recording in Observation Points
The whole set of the OPs was explored during three sampling periods
(November-December 1980, March-April 1981 and June-July 1981). In
each of these periods the OPs were visited sequentially, five per day.
First the OPs of row 7 were visited followed by rows 8, 6, 9, 5 and thus
successively (Figure 2). In each OP, a 45-minute period was spent
constantly walking the streets and recording the number of individuals
of different butterfly species seen. The field data were transferred to
computer cards and all calculated values were obtained through the
use of SPSS (Nie et al., 1975) programs.
160
J.Res.Lepid.
i
Results and Discussion
Distribution of Butterflies along the Transect Routes
Table 1 includes the total number of individuals of different species
along the four transect routes. The recordings for the final 1.6 kilo¬
meters of route AB (8 km in total length) are not included in this table,
since they represent extra-urban data, not comparable to those
obtained for other routes. Figures 3, 4, 5 and 6 show graphic repre¬
sentations of the butterfly groups along the four routes.
From AB to GH there occurs a levelling of topography, an increase of
urbanization intensity and a decrease in the number of individuals
recorded per km of transect (Table 1).
Dryas iulia, Ascia monuste orseis and Phoebis philea were the most
numerous butterflies, totalling 30% of the recorded insects along each
route. The predominance of these species is due, among other factors, to
their great abundance in the region (including within the city), speed
and mobility, and the vivid colors of their wings which allows easy
spotting.
Table 1. Butterflies observed along 20 transect (center-suburbs-center) on
four acess routes. Explanation in the text.
SPECIES
AB
(17.3)*
N %
CD
(14.7)
N %
ROUTE
EF
(11.9)
N %
GH
(10.5)
N %
TOTAL
N %
Dryas iulia (Fabricius, 1775)
88
17.0
63
14.3
46
12.9
26
9.9
223
14.1
Ascia monuste orseis (Latreille, 1819)
65
12.5
55
12.4
49
13.8
32
12.2
201
12.7
Phoebis philea (Johansson, 1763)
44
8.5
45
10.2
47
13.2
21
8.0
157
9.9
Anartia amathea (Eschscholtz, 1821)
23
4.4
24
5.4
22
6.2
49
18.7
118
7.5
PapiUo scamander Boisduval, 1836
22
4.2
27
6.1
25
7.0
15
5.7
89
5.6
Phoebis spp.
21
4.0
22
5.0
23
6.5
17
6.5
83
5.3
Junonia evarete (Cramer, 1779)
25
4.8
19
4.3
16
4.5
21
8.0
81
5.1
Colias lesbia pyrrhothea (Hubner, 1823)
29
5.6
34
7.7
1
0.3
—
-
64
4.1
Tatochila autodice (Huebner, 1818)
30
5.8
14
3.2
9
2.5
1
0.4
54
3.4
PapiUo anchisiades capys Huebner, 1809
30
5.8
15
3.4
8
2.2
-
-
53
3.4
Urbanus spp.
16
3.1
13
2.9
13
3.6
8
3.1
50
3.2
Actinote spp.
6
1.2
18
4.1
7
2.0
13
5.0
44
2.8
Euptychia spp.
6
1.2
4
0.9
14
3.9
16
6.1
40
2.5
Anosia gilippus (Cramer, 1775)
22
4.2
6
1.4
8
2.2
2
0.8
38
2.4
Agraulis vanillae maculosa (Stichel, 1907)
3
0.6
8
1.8
13
3.6
8
3.1
32
2.0
Eurema spp.
9
1.7
6
1.4
10
2.8
1
0.4
26
1.6
Phyciodes spp.
2
0.4
5
1.1
9
2.5
8
3.1
23
1.5
Battus polydamas (Linnaeus, 1758)
12
2.3
3
0.7
2
0.6
—
-
17
1.1
Eunica margarita (Godart, 1822)
9
1.7
5
1.1
1
0.3
2
0.8
17
1.1
Dione juno (Cramer, 1779)
2
0.4
8
1.8
4
1.1
-
-
14
0.9
Methona themisto Huebner, 1818
8
1.5
3
0.7
1
0.3
1
0.4
13
0.8
PapiUo hectorides Esper, 1794
3
0.6
5
1.1
2
0.6
-
—
10
0.6
Biblis hyperia (Cramer, 1779)
3
0.6
-
-
4
1.1
2
0.8
9
0.6
PapiUo thoas brasiliensis Rothschild & Jordan, 1906
5
1.0
2
0.5
-
—
1
0.4
8
0.5
Placidula euryanassa (Felder, 1860)
-
—
4
0.9
1
0.3
3
1.1
8
0.5
Adel p ha spp.
-
-
4
0.9
3
0.8
1
0.4
8
0.5
Heliconius erato phyllis (Fabricius, 1775)
2
0.4
3
0.7
1
0.3
1
0.4
7
0.4
Dryadula phaetusa (Linnaeus, 1758)
1
0.2
-
-
2
0.6
4
1.5
7
0.4
Siproeta stelenes (Linnaeus, 1758)
1
0.2
1
0.2
3
0.8
1
0.4
6
0.4
PapiUo astyalus Latreille, 1819
4
0.8
1
0.2
-
-
—
-
5
0.3
Diaethria spp.
1
0.2
3
0.7
1
0.3
-
-
5
0.3
Doxocopa laurentia (Godart, 1821)
3
0.6
1
0.2
-
—
-
-
4
0.3
Hamadryas amphinome (Fruhstorfer, 1916)
2
0.4
2
0.5
-
-
-
-
4
0.3
Anaea itys (Gmelin, 1791)
1
0.2
1
0.2
1
0.3
1
0.4
4
0.3
Dismorphia spp.
2
0.4
—
-
2
0.6
-
-
4
0.3
Hamadryas spp.
2
0.4
1
0.2
-
-
-
-
3
0.2
Epiphile huebneri Hewitson, 1861
-
-
1
0.2
2
0.6
-
-
3
0.2
Heliopetes omrina (Butler, 1870)
-
-
-
-
1
0.3
2
0.8
3
0.2
Eurema deva deva (Doubleday, 1847)
1
0.2
1
0.2
-
-
1
0.4
3
0.2
Opsiphanes invirae Stichel, 1901
1
0.2
2
0.5
-
-
—
-
3
0.2
Dynamine myrrhina (Doubleday, 1849)
1
0.2
-
-
-
-
1
0.4
2
0.1
Riodina lysistrata (Berg, 1896)
-
1
0.2
-
-
1
0.4
2
0.1
Praepedaliodes phanias (Hewitson, 1861)
1
0.2
-
-
1
0.3
-
-
2
0.1
Mechanics lysimnia (Fabricius, 1793)
2
0.4
-
—
-
-
-
-
2
0.1
Euryades corethrus (Boisduval, 1836)
1
0.2
-
-
-
-
-
—
1
0.1
Pyrgus oileus (Stoll, 1790)
1
0.2
-
-
-
-
—
-
1
0.1
Pyrgus communis (Giacomelli, 1928)
-
—
-
—
-
-
1
0.4
1
0.1
Doxocopa kallina (Staudinger, 1886)
1
0.2
—
-
-
-
-
—
1
0.1
Vanessa braziliensis (Moore, 1883)
1
0.2
-
-
-
-
-
-
1
0.1
Marpesia petreus (Cramer, 1776)
-
—
1
0.2
-
—
-
-
1
0.1
Eypanartia bella (Fabricius, 1793)
-
-
—
-
1
0.3
-
—
1
0.1
Philoros rubriceps opaca (Boisduval, 1870)
-
-
-
-
—
-
1
0.4
1
0.1
Others
7
1.3
11
2.5
3
0.8
-
21
1.3
Total
519
100.0
442
100.0
356
100.0
262
100.0
1579
100.0
(N/Km/TRANSECT)
25(3): 157-178, 1986(87)
161
The papilionids (Figure 3) show a reduction in the number of indi¬
viduals from AB to GH; in the latter transect, except for one individual
of Papilio thoas brasiliensis, all those recorded belonged to the species
P. scamander scamander. This monotony is in accord with the small
number of species of this family observed in the OPs located in this area
of the city.
The sap and fruit eating nymphalids were most common along AB,
also decreasing in the direction of GH (Figure 6). All these species are
native of subtropical woods on the city periphery, showing their
greatest numbers on the distal end of AB, which crosses areas with
remnants of this habitat.
Along the routes AB, CD and EF the different families and subfami¬
lies showed a sharp reduction of the species number and individuals
inside the limits of zone B; only one or two species were recorded for
each group of butterflies. On GH, however, there was a greater
homogeneity in the distribution of these groups, represented all along
the route by the species that on other routes were well represented in
zone B. This emphasizes the environmental stress of this region. The
homogeneity in the distribution of the different groups of butterflies
along GH is probably due in part to the spatial uniformity of this
portion of the city. This area has a very regular disposition of streets,
similar to a chessboard, and is extremely flat with elevations below 5
meters, which represents a low diversification of habitats. In aerial
photographs it shows great similarity among its different sites. The
scarcity of vegetation on the margins of route GH tends also to increase
the homogeneity in the distribution of butterflies, since it eliminates a
factor of concentration of these insects. Farrapos Avenue, the greatest
part of route GH, is surely the avenue with the greatest air pollution in
the city due to particles and industrial gases as well as from vehicles.
Pollution is a factor of homogenization of environmental conditions
consequently decreasing the complexity of animal and plant communi¬
ties belonging to a certain biotope. Thus, the smaller species number
and homogeneity of distribution found along GH may also be explained
by the air pollution in this area.
The Urban Community of Butterflies
The data in Table 2 show the large number of individuals of a small
number of butterfly species in the urban area. The data provide
evidence that the butterfly communities of Porto Alegre are organized
with a consistent structure. This can be seen from the results of the two
methods used. For example, the more abundant species in the transects
and OPs hold the top positions in the abundance ranking in the
majority of routes and regions of the city (Tables 1 and 2). The majority
of the genera and species which represent less than 2% of the records in
the transects maintain this low proportion also in the OPs. It will be
162
J. Res. Lepid.
Table 2. Total number of butterflies observed in 11 regions of the city of
Porto Alegre.
REGIONS
IV V VI VII VIII IX X XI
Ascia monuste orseis (Latreille. 1819)
Dryas iulia (Fabricius, 1775)
Junonia evarete (Cramer, 1779)
Urbanus spp.
Tatochila autodice (Huebner. 1818)
Phoebis philea (Johansson, 1763)
Papilio scamander Boisduval. 1836
Papilio anchisiades capys Huebner, 1809
Actinote spp.
Agraulis vanillae maculesa (Stichel. 1907)
Anosia gilippus (Cramer, 1775)
Phoebis spp.
Eurema spp.
Battus poiydamas (Linnaeus, 1758)
Euptychia spp.
Anartia amathea (Eschscholtz, 1821)
Papilio astyalus Latreille. 1819
Heliopetes omrina (Butler, 1870)
Leptotes cassius (Cramer, 1775)
Papilio thoas brasiliensis Rothschild & Jordan, 1906
Methona themisto Huebner, 1818
Vanessa braziliensis (Moore, 1883)
Phyciodes daudina (Eschscholtz, 1821)
Euryades corethrus (Boisduval, 1836)
Papilio hectorides Esper, 1794
Heliopetes alana (Reakirt, 1868)
Eurema deva (Doubleday, 1847)
Dione juno (Cramer, 1 779)
Fergus oileus (Stoll, 1780)
Eunica margarita (Godart, 1822)
Heliconius erato phyllis (Fabricius, 1775)
Parides perrhebus (Boisduval, 1836)
Pyrgus communis (Giacomelli, 1928)
Colias lesbia pyrrhothea (Hiibner, 1823)
Euptoieta hortensia (Blanchard. 1852)
Hamadryas spp.
Dryadula phaetusa (Linnaeus, 1758)
Placidula euryanassa (Felder, 1860)
Dynamine myrrhina (Doubleday, 1849)
Anaea itys (Gmelin, 1791)
Parides agavus (Drury, 1782)
Adelpha spp.
'Philoros rubriceps opaca (Boisduval, 1870)
Biblis hyperia (Cramer, 1779)
Eurytides lysithous (Huebner, 1821)
Praepedaliodes phanias (Hewitson, 1861)
Diaethria spp.
Phyciodes ithra (Kirby, 1900)
Riodina spp.
Dismorphia spp.
Doxocopa laurentia (Godart, 1821)
Battus polystictus (Butler, 1874)
Siproeta stelenes (Linnaeus, 1758)
* Josia angulosa (Walker, 1854)
Hypanartia bell a (Fabricius, 1793)
Hamadryas amphinome (Fruhstorfer, 1916)
Doxocopa kallina (Staudinger, 1886)
Opsiphanes invirae Stichel, 1901
Parides anchises nephalion (Godart, 1819)
* Phaloe cruenta (Huebner, 1823)
• Utetheisa ornatrix (Linnaeus, 1758)
Prittvyitzia hymenaea (Prittwitz, 1865)
Phyciodes lansdorfi (Latreille, 1820)
Siproeta trayja (Hiibner, 1823)
Marpesia petreus (Cramer, 1776)
Morpho catenarius Perry, 1811
Anartia jatrophae (Johansson, 1763)
Philaethria wernicket (Rober, 1906)
'Macrocneme chrysitis (Guerin, 1843)
Epiphile huebneri Hewitson, 1861
Others
117
152
44
49
63
76
23
45
47
21
62
29
42
64
24
17
18
15
26
7
24
19
5
12
12
8
29
33
2
3
18
6
10
3
21
9
9
6
6
7
3
2
3
10
2
7
2
2
5
2
1
1
3
2
40
100 111 138 102
145 96 1 54 120
46 122 62 83
116 117 69 74
84 55 57 74
86 60 57 43
48 94 13 34
73 84 48 64
67 93 28 70
67 54 47 59
34 46 45 30
61 51 37 38
36 45 36 38
26 48 50 41
31 28 15 25
21 33 10 7
22 31 33 22
21 21 12 19
24 20 36 19
18 15 13 18
16 11 14 13
5 49 6 12
18 24 19 28
8 50 17 12
7 25 9 26
10 25 15 23
12 12 11 12
10 7 11 14
13 13 12 20
9 9 10 5
4 4 12 15
6 4 4 13
8 12 9 14
2 3 4 1
7 21 2 8
6 1 6 10
18 6 1 -
8 3 9 9
4 2 3 3
5 8 11
- - - 3
4 111
2 3 4 3
13 1-
3 14 4
6 112
2 2 1-
2 111
1-31
13 2 2
4 - 2 -
2 1-3
2 - - 2
2 1
1 2
80
56
70
64
55
29
29
23
16
59
23
27
35
19
27
46
10
30
20
5
21
24
14
28
6
17
7
2
5
3
2
9
3
2
90
109
99
80
47
67
62
39
69
21
44
37
24
36
22
13
15
17
25
22
10
17
7
6
17
9
16
5
8
10
9
2
3
4
2
5
3
2
3
80 58
62 37
64 110
61 59
43 45
62 12
51 72
30 37
25 7
34 11
62 40
40 12
41 21
16 12
17 19
56 11
12 25
28 11
9 10
13 15
16 19
12 7
3 3
13 1
12 1
16 5
7 9
1 3
3 2
7 2
3 38
5 1
2
2 2
2
2
2
2 1
2
1 1
3
70
33
39
43
53
26
12
17
49
14
15
7
3
10
13
18
16
3
1
6
10
3
2
65
17
48
30
30
22
41
15
2
6
7
2
12
2
4
6
10
j
2
5
2
5
2
33 34 38 40 39 29 30 35 7 11
138
130
126
104
103
93
86
66
63
61
56
51
45
42
29
26
24
21
21
20
20
16
15
14
14
10
9
8
7
7
6
6
5
4
3
3
2
2
2
2
336
8.71
8.39
6.82
6.48
5.10
4.80
4.48
4.35
3.74
3.63
3.49
3.32
2.68
2.58
2.22
2.14
1.69
1.58
1.56
1,41
1.34
1.33
1.20
1.19
1.12
1.09
1.02
0.90
0.89
0.80
0.74
0.57
0.54
0.48
0.44
0.39
0.36
0.25
0.22
0.21
0.18
0.18
0.17
0.17
0.16
0.14
0.13
0.12
0.12
0.09
0.08
0.07
0.06
0.05
0.05
0.05
0.04
0.03
0.03
0.03
0.03
0.03
0.02
0.02
0 02
0.02
2.89
Total
1392 1369 1568 1198 1291 950 1128 970 767 583 394 11610 100.00
* moths
shown below that this consistent organization may also be applied to
the distribution of the members of this fauna.
Figures 7 — 10 show the distribution of the different groups of butter¬
flies in the urban zones. These maps may be seen as an estimate of the
distribution areas of different species in the urban area of Porto Alegre
for the period of 1980—81; this is certainly suffering gradual modifica¬
tions, considering the velocity of vertical and horizontal urbanization.
Within each subfamily or genus of butterflies there are species spread
out over all zones of urbanization and others found in semi-circular
bands progressively narrower and farther from the zones B and HB
having as virtual center zone B. This fact is related to the radial
character of the urbanization gradient and vegetation covering of the
city. The majority of the species show a continuous distribution over
the city, decreasing in amplitude towards more intensively urbanized
zones. This, along with the high degree of vagility of the dominant
25(3): 157-178, 1986(87)
163
species (and the majority of others) discourages the use of the express¬
ion mosaic distribution (often applied to soil insects) for the butterfly
fauna of Porto Alegre. The expression life zones introduced by Merriam
(1894) to designate the changes of plant communities due to altitude
and latitude better characterizes the zonation of the butterfly distribu¬
tion on the urban gradient.
Each species shows a more or less similar distribution pattern in the
three samples, though some members of the subfamily Nymphalinae
reveal seasonal variations in their distribution. In each case the pat¬
tern of distribution verified in the transect routes was in general
similar to the one found for the OPs. The species that showed a rather
wide distribution in the OPs (such as P. scamander, A. m. orseis and D.
iulia ) also showed a wide distribution along the routes of transects. The
species with a more restricted distribution in the OPs such as P. a.
astyalus, P. hectorides and H. e. phyllis were found to be more frequent
on the outer portions of the routes. The species observed only on the
border of urban area ( B . polystictus, P. a. nephalion and P. agauus ),
within areas not reached by the majority of the routes were very
infrequent along the transects. Neverthless, they were found on the
distal end of route AB which reaches the city periphery. These facts
emphasize the zonation of distribution areas of butterflies in the urban
area of Porto Alegre.
The species that were rare in the urban area (less than 1%) in general
are stenotopic in the sense of the adult being typical of field or woods.
They feed in the larval stage on native plants which are infrequent or
non-existent in the city. Their distribution was restricted to peripheral
portions of zone H, especially in the southern sector which is richer in
remnants of subtropical woods and is nearer the granitic hills of the city
periphery, where still denser woods are located. In the adult stage fruit
and sap feeding is predominant.
In the central areas of the city, species of open areas predominate, in
accord with the results of Yamamoto (1977) on the butterflies of
Sapporo (northern Japan). Species typical of natural fields behaved in
Porto Alegre much like the woods species, even though they were more
numerous; their distribution was concentrated in zone H.
The drying and warming of the urban environment makes the habi¬
tats of green areas similar to the xerothermic ones (Schweiger, 1953;
Trojan, 1981) favoring species which tolerate low humidity and sub¬
light (Kouch & Sollmann, 1977; Pisarski & Czechowski, 1978). Many
forest species show a preference for rather low temperatures, high
humidity and shade. On the contrary the field species prefer high
temperatures, low humidity and sunlight (Tischler, 1965). Naturally,
the ecology of a butterfly species in the city and its success in adapting
to this new environment are directly related to its ecology in natural
conditions. Thus the lepidopteran species typical of fields would be
better pre-adapted to urban life than forest species.
164
J.Res.Lepid.
If cities are considered as well illuminated open areas, warm and with
low humidity, it would be reasonable that field species would be
dominant in central areas of Porto Alegre; instead, they are lacking
there, since natural fields are not present. The predominant physiog¬
nomy of urban habitat is closer to a savanna, with open areas where a
low vegetation can grow (in general subjected to some form of manage¬
ment), consisting of shrubs and trees interspersed by built-up areas.
From this fundamental character of the urban habitat probably comes
the predominance in urban Porto Alegre of species that are not typical
either of fields or woods but prefer open areas. They are eurytopic in
the sense that the adults may be observed either in grasslands or in
woods or mixed areas. In the larval stage they utilize native and exotic
plants widely spread over the town. The available adult and larval food
apparently is the main biotic ecological factor that explain the great
abundance of the dominant butterflies in the urban area of Porto
Alegre (Ruszczyk, 1986). Typical of these species is their degree of
vagility, which certainly has contributed to their wide distribution in
the city.
The Abundance of Butterflies in the Urbanization Zones
Figure 11 shows the number of butterflies recorded in the three
samples of the urban area of Porto Alegre. All samples reveal a
progressive reduction of the number of individuals in the direction of
zone B. The mean number found for zone B was about 40 individuals,
compared with about 64 in zone HB and about 130 in zone H. There is
thus an increase of 60% from zone H to zone HB and more than 100%
going from zone HB to H. This last increase already appeared in the
OPs of zone HB located on the border of zone H (Figure lid). The
border between zone H and zone HB acts as a barrier for several
butterfly species, especially those characteristic of field and wood
environments. This border is the main transition area of the butterfly
fauna in going out from the central area of the city. Its presence was
obvious on the maps showing the number of individuals sampled in
summer, winter and total seen as well as on diversity maps (in prep.).
This border is also important for some bird species that are sensitive to
urbanization (Ruszczyk et al., 1987).
The relative influence of the variable plant cover, distance from the
city center and mean altitude of the OPs was analyzed for the total
number of butterflies recorded, through simple correlation and multi¬
ple regression methods. The three variables showed positive correla¬
tions with the total number of butterflies, with the respective coef¬
ficients being 0.714, 0.710 and 0.456 (all significant to the 1% level).
Standardization of variables gave a standard regression coefficient of
0.326 for plant cover, 0.433 for distance from the city center and 0.154
for mean altitude, all significant to the 1% level. This indicates that the
25(3): 157-178, 1986(87)
165
distance from the city center has a greater influence on the number of
individuals than the plant cover or mean altitude. These three vari¬
ables together were responsible for 61% of the explained variance of the
total number of recorded butterflies for each OP. Decomposing this
proportion shows the contribution of each variable:
Proportion
Increment
Increment
Increment
Not attributed
of variance
due to the
due to
due to
to either
explained by
distance
plant
average
Xx, X2 or X3
all three
from the
cover
altitude
alone
variables
center of
the city
(In km)
(arc sine V%)
(m)
(R2)
(XJ
(X2)
(X3)
0.610
= 0.092
+ 0.041
+0.017
+0.460
Three quarters of the explained variance in the recorded number of
butterflies is due to secondary effects between variables. The predomi¬
nance of the single variable distance over plant cover and altitude is
probably related to the large number of other variables which are
directly related to it and are important to the butterflies. Variables
such as temperature of the urban area, percent plant cover, degree of
habitat disturbance (movement of vehicles and human beings), human
population density, air pollution and intensity of urbanization are all
organized as predominantly radial gradients due to the fundamental
radial character of Porto Alegre’s urbanization. In this way the intensi¬
ty of action of these and other variables (which may be called all
together anthropogenic pressure (Trojan, 1981)) on the lepidopterans
depends in great portion on their position relative to the center of the
city. This suggests a predominance of effects of physical factors on the
distribution of these insects in urban areas (but see Ruszczyk, 1986 for
a discussion of biotic factors in one common species, Papilio scaman-
der).
Acknowledgments. I wish to acknowledge with thanks the financial support
provided by Conselho Nacional de Desenvolvimento Cientifico e Tecnologico
(CNPq). I would like to thank Aldo Mellender de Araujo, Keith S. Brown, Jr
and Miriam Becker for helpful criticisms and suggestions. Celso Paulo Jaeger
kindly prepared the first English version of the paper.
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Entomology. New York, Academic. Press, p. 1-12.
TISCHLER, W., 1965. Agrarokologie. Jena, G. Fischer.
TROJAN, P., 1981. Urbanfauna: faunistic, zoogeographical and ecological prob¬
lems. Memorab. zool., 34: 3—12.
YAMAMOTO, M., 1977. A comparison of butterflies assemblages in and near
Sapporo city, northern Japan. J. Fac. Sci. Hokkaido Univ. Serie 6, Zoology,
20(4): 621-646.
25(3): 157-178, 1986(87)
167
Figure 1. a) Schematic map of ecosystems within and around the city of
Porto Alegre.
1. urban area; 2. agriculture; 3. agriculture and livestock; 4.
agriculture and second growth; 5. marshes; 6. subtropical forest.
b) Map of percent plant cover of PA.
c) Map of urbanization zones of the city (1978).
d) Simplification of map "c" .
168
J. Res. Lepid.
ABCDEFGH I JKLMN
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
Figure 2. Location of the 1 1 1 observation points of the butterfly fauna of the
city of Porto Alegre. Each observation point has a diameter of 600
m and its area was sampled three times for butterflies. The
dashed line corresponds to the simplified limit of the urban area.
Solid lines demarcate 11 regions into which the observation
points were grouped for analysis.
25(3): 157-178, 1986(87)
169
0*1
•8*00*a O
1 K M
S . . o. . o
•080 ^ o* 08 •
o y 9 O 8 c&
o o
o
&
•-P A. CAPYS
5m O- P T. BRASILfENSIS
] H
m
9- P A. ASTYALUS
▼ - P HECTOR IDES
A-BATTUS polydamas
O-Parides PERRHEBUS
□- P AGAVUS
Figure 3. Family Papilionidae — Distribution in the urbanization zones of
Porto Alegre. Five transects center-periphery-center (1, 2, 3, 4, 5)
were made on each route in April and May 1980, February, April
and May 1981, respectively. The line under the symbols is the
topographic profile of the routes. The urbanization zones crossed
by the routes (see map at lower right) are indicated under the
topographic profile.
1. buildings zone; 2. houses and buildings zone; 3. houses zone;
4. houses zone with remnants of subtropical forest.
170
J.Res.Lepid.
• - A S C I A M. ORSEIS
O-PHOEBIS PHI LEA
9-EUREMA SPP.
1km
Figure 4. Family Pieridae — Distribution in the urbanization zones of Porto
Alegre. See legend of Figure 3.
z’ z
25(3): 157-178, 1986(87)
171
1 o
2 K7
3
4 O O O o o
5 o o co o o o
o o 8b o
O o CD
• o
o o o &>o ooA> o o
o 008 o o o o
8 o cBa o
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B
O-DRYAS JULIA
•-AGRAULIS V. MACULOSA
A- DlONE JUNO
<7- Helicon ius e. phyllis
©- Dryadula phaetusa
1 K M
□
Figure 5. Family Nymphalidae (Heliconiini) — Distribution in the urbaniza¬
tion zones of Porto Alegre. See legend of Figure 3.
172
J.Res.Lepid.
o.
. <£ ••
2
2 ©
3 OOOOOO *0*0 o oo8fio
4 o oo o oo • o» o •
5oOO ^7 00 Q • o o oo
G |inn7;=i;;=;;;;.:i=:;;:-::i:i-:i:i:l5.;=::|||||H|||||H|||l||H|m|[H||H|U||H|||l||HlllllllllllllHIIII I H
1 K M
O - A NARTIA A M ATM EA
• - JUNONIA EVARETE
S7- BlBLIS HYPER IA
a - Doxocopa spp.
©- Adelpha spp.
O-Diaethria spp.
□ - A N A E A ITYS
A- Hamadryas SPP.
Figure 6. Family Nymphalidae (Miscellanea) — Distribution in the urbaniza¬
tion zones of Porto Alegre. See legend of Figure 3.
25(3): 157-178, 1986(87)
173
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0©0©'Ab'@®®
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Figure 7. Family Papilionidae — Distribution in the urbanization zones of
Porto Alegre. The butterfly fauna of 1 1 1 observation points of the
urban area was sampled three times, in November-December
1980, March-April 1981 and June-July 1981, respectively 1, 2 and
3.
174
J. Res. Lepid.
I
25(3): 157-178, 1986(87)
175
/©- a/ Av&tA Af
A © A @
@ A A A © ® ©
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y ©©©/
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Figure 9. Family Nymphalidae (Heliconiini) — Distribution in the urbaniza¬
tion zones of Porto Alegre. See legend of Figure 7.
25(3): 157-178, 1986(87)
177
/©- a/ ^a\©k
A A A(>A.A^
/AAAA-A AJ<$@'
aaa a a?a a'©Ta a"'
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Figure 10. Family Nymphalidae (Nymphalinae) — Distribution in the urba¬
nization zones of Porto Alegre. See legend of Figure 7.
178
J. Res. Lepid.
Figure 11. Number of butterflies registered during three samples in 111
observation points of the urban area of Porto Alegre. In each
observation point a period of 45 min was spent walking an urban
area of 600 m in diameter and recording the butterflies seen. 1,
0-16 individuals; 2, 17-40; 3, 41-70; 4, 71-100; 5, 101-135.
Journal of Research on the Lepidoptera
25(3): 179-187, 1986(87)
The Effect of Temperature on Expression of the Dark
Phenotype in Female Papilio glaucus (Papilionidae)
David B. Ritland
Department of Zoology, University of Florida, Gainesville, Florida 32611
Abstract. Experimental broods of Papilio glaucus produced unusual
dark morph females when reared at high temperatures. Exposure to
temperatures of 25-28 C during the larval and pupal stages produced
adult females which were phenotypically intermediate between the
normal yellow and dark morphs of the butterfly, i.e., with a dusting of
yellow scales in the dark background. Naturally-occurring females
with this intermediate coloration have been recorded from throughout
the eastern United States, but are generally infrequent. The dark
morph of Papilio glaucus appears to be canalized (buffered) against
environmental modification under natural conditions. It is proposed
that canalization of the dark morph is adaptive because it protects the
mimetic resemblance of dark females to the unpalatable Battus
philenor, and that canalization is strongest in populations of P.
glaucus from areas where B. philenor is an abundant model.
Introduction
Phenotypic plasticity and polyphenism (Shapiro, 1976) in butterflies
are presumably adaptive responses to heterogeneous or seasonal en¬
vironments. However, developmental canalization (inflexibility of the
normal phenotype over a range of environmental conditions due to the
action of the epigenetic system; Waddington, 1957) is also adaptive
(Shapiro, 1981; Hoffman, 1982). Phenotypic stability may be particu¬
larly advantageous in mimetic species, because environmental mod¬
ification of the wing pattern would decrease the mimetic resemblance.
This paper summarizes an investigation into phenotypic plasticity and
canalization in the mimetic eastern tiger swallowtail, Papilio glaucus
L.
Two subspecies of the tiger swallowtail, P. g. glaucus L. and P. g.
australis Maynard, exhibit a female sex-limited wing color dimorphism
(The dimorphism does not occur in P. g. canadensis Rothschild &
Jordan). One female form resembles the male in having the typical
pattern of a black-banded yellow background; the other female form is
heavily melanized, with the banding pattern virtually obscured by dark
scales. The dark female morph is thought to mimic the unpalatable
Battus philenor (L.) ( e.g ., Brower, 1958), and while both dark and
yellow female morphs occur throughout the eastern U. S., the dark
form is more frequent where Battus philenor is abundant (Brower and
Brower, 1962).
180
J.Res.Lepid.
Clarke and Sheppard (1957, 1959, 1962) and Clarke et. al. (1976) have
provided compelling evidence that melanism in Papilio glaucus is
controlled by a female-limited gene, presumably associated with the Y
(W) chromosome. This is supported by the absence of the melanic form
in males, and the fact that in virtually all cases, females produce
daughters of the same color morph as themselves. Rare exceptions do
occur in which both yellow and dark female progeny arise from a single
mother ( e.g ., Edwards, 1884; Weed, 1917; Clarke and Sheppard, 1959).
Classically, these mixed broods have been regarded as the result of
abnormalities in chromosome architecture or meiotic processes, but a
novel explanation for certain cases was suggested by Scriber and
Ritland (in press). These authors described a genetic component in the
monomorphic subspecies P. glaucus canadensis that completely sup¬
presses phenotypic expression of the dark morph in hybrid offspring
from laboratory crosses between male P. g. canadensis and dark morph
female P. g. glaucus. Scriber and Ritland argued that in some cases,
anomalous dark morph inheritance patterns may be the result of
natural hybridization between P. g. glaucus and P. g. canadensis. The
rare occurrence of analagous mutant alleles in P. g. glaucus and P. g.
australis may explain other cases of unusual inheritance.
Occasionally, Papilio glaucus females exhibit wing patterns in¬
termediate between the normal yellow and dark morphs (i.e., with a
dusting of yellow scales in the dark background). The occurrence of
yellow-dark intermediate individuals is an entirely separate phe¬
nomenon from the mixed broods described above. The intermediate
female phenotypes are poor mimics of Battus philenor; Clarke and
Sheppard (1959) postulated the presence of an efficient genetic “switch
mechanism” in P. glaucus (presumably a single gene controlling mela-
nization) which prevents the occurrence of these nonmimetic in¬
termediates. Intermediate females of P. glaucus with significant yellow
suffusion of the dark background are uncommon, but have been
recorded from many areas in the eastern United States: New York
(Edwards, 1884; Shapiro and Shapiro, 1973); New Jersey (Clarke and
Clarke, 1983); Ohio (M. H. Evans, pers. comm.); West Virginia (Ed¬
wards, 1884); Virginia (Clark and Clark, 1951); Maryland (Clark and
Clark, 1932); Pennsylvania (Shapiro, 1966; Ehle, 1981); Wisconsin
(pers. obs); Mississippi (B. Mather, pers. comm.); Kentucky (pers. obs.);
Georgia (Harris, 1972); and Florida (pers. obs.). Dark morph females
with at least a slight suffusion of yellow scales probably occur in low
frequency throughout the eastern United States.
The general rarity of intermediate females in wild populations sug¬
gests that the dark mimetic phenotype of P. glaucus is strongly
canalized (buffered) under normal environmental conditions. In¬
termediate females may arise because of either genetic shock (e.g.,
mutant alleles or incomplete penetrance/expressivity of normal alleles
controlling melanization) or environmental shock (disruption of the
25(3): 179-187, 1986(87)
181
canalized developmental pathway by unusual environmental condi¬
tions). The present study investigates phenotypic plasticity in dark
morph Papilio glaucus females as a function of one environmental
variable, temperature. Phenotypic plasticity and canalization of the
dark morph are discussed in relation to mimicry in this butterfly. I
hypothesize that canalization of the dark morph is adaptive because it
stabilizes the mimetic resemblance to Battus philenor, and that phe¬
notypic stability may be more strongly selected for in areas where B.
philenor is an abundant model.
Methods
Experiments conducted in 1981, 1983 and 1984 investigated the effect
of rearing temperature on wing coloration in samples of Papilio glaucus
from eight geographic areas: Dane County, WI; Dauphin County, PA;
Adams County, OH; Mercer County, WV; Bell County, KY; Jefferson
County, AL; Oconee County, GA; and Alachua County, FL. Laboratory
cultures were established and ova for the study were obtained from
dark morph females which had been mated to male siblings by the
hand-pairing method of Clarke and Sheppard (1956). Females ovipo¬
sited on foodplant leaves in plastic shoeboxes warmed by incandescent
lights.
Newly-eclosed larvae were transferred to environmental chambers
and reared at one of three constant temperatures: 22, 25, or 28 C.
Temperature readings taken at different locations within each cham¬
ber indicated fluctuations of less than 0.5 C. All treatments were
maintained at a photoperiod of 16L:8D to inhibit diapause and to
remove photoperiodic variability as a relevant factor. The larvae were
fed leaves on excised twigs of Black Cherry, Prunus serotina Ehrh.
Foodplant turgidity was maintained by placing the twigs in Aquapics.
Pupae were kept in individual screen cages at the larval rearing
temperature.
All female progeny from this experiment were expected to exhibit the
normal dark morph phenotype. To describe deviation from the normal
dark pattern, the dorsal background color of each reared female was
scored relative to a group of five reference specimens. These reference
specimens represent five points on a continuum ranging from a normal
dark morph female (assigned a rating of ‘O’) to an intermediate
yellow-dark phenotype (rating = 4) which has a heavy suffusion of
yellow dusting in the dark background, giving the butterfly a ‘sooty’
appearance (Figure 1). Reared females were compared to this reference
group and assigned an appropriate score. The rating scale ranged by
half steps from 0 to 4.
The modification of the dark morph pattern at different rearing
temperatures was investigated statistically via the Kruskal- Wallis
one-way ANOVA for ordinal data (Siegel, 1956). This procedure com-
182
J. Res. Lepid.
Figure 1. Reference specimens of Papi/io g/aucus showing grading scale
used to quantify dorsal wing color of experimental specimens.
pared median color rating among the three rearing temperatures
within each geographic sample.
Results
A total of 281 dark morph females from the eight geographic samples
were scored for dorsal wing background color. Table 1 presents the
median color ratings and range of individual scores for each geographic
sample at three rearing temperatures and the associated statistics.
These data indicate that higher color ratings (greater suffusion of
yellow scales in the dark background) occurred under high rearing
temperature regimes; i.e., there was significant modification of dark
morph expression at 28 C relative to the two lower temperatures. In
addition, the eight geographic samples differ significantly from one
another in the degree of phenotypic modification at 28 C (Kruskal-
Wallis ANOVA, H = 9.4, p < .01).
Intrasample variability is relatively high at 28 C: most samples reared
at this temperature contained individuals ranging over at least two full
steps on the color scale (Table 1). Such individual variation in suscepti¬
bility to environmental modification (or canalization of the normal dark
color pattern) may represent individual differences in the suite of
modifier genes which protects the normal phenotype (Waddington,
1961). Wing pattern elements other than the melanic background ( e.g ,
25(3): 179-187, 1986(87)
183
Table 1. Median color scores and range of individual values for eight
samples of dark female PapiHo g/aucus reared at three constant
temperatures. Kruskal-Wallis test statistic (H) and significance
level for differences in color rating among the three temperatures
are indicated for each sample.
22 C
25 C
28 C
Sample
median (range)
median (range)
median (range)
H
P
Wl
0.0 (0.0-0.0)
0.0 (0.0-0.5)
3.0 (1. 0-4.0)
16.5
.001
OH
0.0 (0.0-0.0)
0.0 (0.0-2. 0)
0.5 (0.0-3.5)
8.9
.05
PA
0.0 (0.0-0.0)
0.0 (0.0-0.0)
1.8 (0.0-2.5)
21.4
.001
AL
0.0 (0.0-0.0)
0.0 (0.0-0.0)
0.8 (0.0-1.0)
11.5
.01
WV
0.0 (0.0-0.0)
0.0 (0.0-0.0)
0.3 (0.0-2.5)
4.4
.20 (N.S.)
KY
0.0 (0.0-0.0)
0.5 (0.0-2.0)
2.0 (1.0-2. 5)
8.8
.05
GA
0.0 (0.0-0.0)
0.3 (0.0-0. 5)
0.5 (0.0-3. 5)
12.5
.01
FL
0.0 (0.0-0.0)
0.0 (0.0-1.0)
0.0 (0.0-3.0)
12.1
.01
the “tiger” stripes and wing margin borders) were virtually unaffected
by temperature. The yellow fore wing discal spot present in some
females (see Figure 1) becomes more pronounced at higher rearing
temperatures (Ritland, 1983), but varies independently of melanic
background color in individual butterflies.
Discussion
Constant rearing temperatures of 25 and 28 C destabilized the dark
morph phenotype of Papilio g. glaucus and P. g. australis. A previous
experiment (Ritland, 1983) suggested that pattern development is
susceptible to temperature modification only during the pupal stage;
this is consistent with the suggestion (Clarke and Clarke, 1983) that
the melanic background pattern develops just before adult eclosion.
The physiological basis of aberrant intermediate pattern development
is not known, but many processes involved in wing pattern develop¬
ment (including pigment synthesis, wing scale maturation, and hor¬
monal control systems) are subject to modification by temperature
(Goldschmidt, 1938; Hintze-Podufal, 1977; Nijhout, 1980). The temper¬
ature sensitivity of tyrosinase-mediated melanization processes in par¬
ticular is well known (Waddington, 1961; Fuzeau-Braesch, 1972; Ma-
jerus, 1981), and high rearing temperatures may also disrupt the
pteridine pigment system involved in P. glaucus pattern development
(Oldroyd, 1971).
Aberrant intermediate phenotypes were expressed only in individuals
reared at 25 C and above, suggesting the existence of a temperature
threshold above which canalization of the normal dark phenotype
breaks down. Developmental pathways are protected by such
genetically-determined thresholds (Waddington, 1961), thereby cana¬
lizing the normal phenotype over a wide range of natural conditions.
This experiment did not investigate photoperiodic effects on pattern
modification in Papilio glaucus , but photoperiod is potentially relevant
184
J . Res. Lepid.
i
in the field. Long and short photoperiods induce different seasonal
forms and aberrations in many butterfly species (e.g., Ae, 1957; Pease,
1962; Fukuda and Endo, 1966; Shapiro, 1976; but cf. McLeod, 1968 and
Lewis, 1985 re species which are insensitive to photoperiodic manipula¬
tion).
The genetic capability to produce the intermediate phenotype repre¬
sents a component of the P. glaucus genome which is not normally
expressed, probably due to a combination of the genetic switch mechan¬
ism proposed by Clarke and Sheppard (1959) and developmental cana¬
lization. While the experimental conditions of this study (24 hr thermo¬
period -I- 16:8 photoperiod) do not represent natural conditions, the
range of rearing temperatures certainly lies within natural limits. This
experiment is therefore qualitatively different from “shock” studies, in
which newly-formed pupae are exposed to extreme heat or cold. Such
shock treatments can produce striking pattern modifications, but also
kill or cripple the majority of individuals, suggesting that critical
developmental pathways are disrupted. Changes in wing pattern in¬
duced by such radical conditions may be of questionable ecological
relevance. In sharp contrast to shock studies, the relatively mild
conditions of the present investigation produced aberrant wing pat¬
terns but did not significantly reduce survival or adult viability (no
significant difference in viability among the three temperature regim¬
es; chi-square p < .01). It is significant that such moderate ex¬
perimental conditions could produce such extreme phenotypic modifica¬
tion, given the fact that intermediates are so uncommon in the wild.
This intriguing situation is similar to that described by McLeod (1968),
who found that the African nymphalid Precis octavia, which exhibits
discrete seasonal forms in nature, produced a wide variety of in¬
termediate forms in his laboratory temperature studies.
Environmental modification of wing pattern may disrupt mimicry in
dark morph Papilio glaucus females; the intermediate phenotypes
produced at 25 and 28 C appear to be very poor mimics of Battus
philenor. The eight geographic samples in this study differed signi¬
ficantly in expression of the intermediate phenotype at 28 C (Table 1).
Both the proportion of aberrant individuals and the degree of phenoty¬
pic alteration varied between samples. Samples from the periphery of
the dark morph range, where Battus philenor is uncommon {e.g.,
Wisconsin and Pennsylvania) were relatively susceptible to tempera¬
ture modification (as indicated by the high median color ratings at 28
C). In contrast, samples from areas where B. philenor is abundant
(West Virginia, Georgia, Alabama, north Florida) seemed to be more
strongly canalized (buffered) against environmental modification. The
West Virginia sample, in fact, showed no evidence of phenotypic
modification by temperature.
These results are consistent with the hypothesis that canalization of
the dark morph is adaptive because it stabilizes the mimetic color
pattern, and that the dark phenotype is most strongly canalized in
25(3): 179-187, 1986(87)
185
areas where it confers the greatest mimetic advantage, i.e., where
Battus philenor is abundant as a model. In regions where B. philenor is
rare and is therefore not an effective model, the selective advantage of
the dark morph relative to the yellow morph is decreased; selection for
genetic modifiers which canalize the dark morph developmental path¬
way should also be reduced. It is significant that many of the records for
wild intermediates occur near the periphery of the dark morph range,
where B. philenor is rare.
The occasional occurrence of wild intermediates of P. glaucus may be
due to either environmental influences (environmental shock) or direct
genetic control (genetic shock). Microhabitat selection by pupating
larvae (e.g., West and Hazel, 1979) may occasionally result in exposure
to high temperatures which disrupt the normal dark morph develop¬
mental pathway and cause expression of the intermediate phenotype.
Alternatively, mutant alleles may alter the canalization threshold of
the normal dark morph (i.e., change the developmental pathway), such
that the intermediate phenotype is expressed under normal environ¬
mental conditions. Such alleles might be related to the gene(s) in P.
glaucus canadensis that inhibit expression of the normal dark morph
(Scriber and Ritland, in press). Similar inhibitory genes have been
described in Papilio rutulus ; hybrid crosses between male P. rutulus
and dark morph female P. glaucus produce intermediate daughters
(Clarke and Willig, 1977) that resemble the environmentally-produced
intermediates (phenocopies) described in this study.
The interaction of genetic and environmental factors affecting pattern
development in Papilio glaucus may significantly alter the resembl¬
ance to Battus philenor. The data presented in this paper support the
hypothesis that canalization of the dark female morph stabilizes the
mimetic color pattern under normal environmental conditions, and
that geographic variation in the degree of phenotypic canalization is
correlated with the abundance of Battus philenor.
Acknowledgements. The author gratefully acknowledges the insightful con¬
tributions of J. M. Scriber, Walter Goodman, and Robin L. Ritland. I am
especially grateful to Lincoln P. Brower for extensive comments, and to Arthur
M. Shapiro and Thomas C. Emmel for very helpful perspectives. Mark Evans,
Robin Ritland, and Jane Schrimpf provided invaluable assistance in the labora¬
tory. This study was funded in part by grants from the National Science
Foundation (DEB 7921749, BSR 8306060 to J. M. Scriber) and the University
of Wisconsin, Madison (Hatch Project 5134).
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!
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Journal of Research on the Lepidoptera
25(3): 188-201,1986(87)
Chromatic Polymorphism in Callophrys mossii bayensis
Larvae (Lycaenidae): Spectral Characterization, Short-
Term Color Shifts, and Natural Morph Frequencies
Larry Orsak1
and
Douglas W. Whitman2
Dept. Entomological Sciences, University of California, Berkeley, CA 94720
Abstract. A tristimulus colorimeter and UV-VIS spectrophotometer
supplemented visual assessments of color polymorphism in wild fourth
instar larvae of the endangered butterfly Callophrys mossii bayensis.
Wild larvae are of many color hues; this contrasts with the distinct
morphs reported from laboratory rearings. Larval color changed over
short time periods when fed yellow flowers or red bracts. The precise¬
ness of visual color matching between larvae and plant substrates is
higher for red than for yellow larvae. This crypsis does not extend to any
precise mimicry of spectral reflectance. Genetic color-determining
mechanisms seem to be supplemented by an environment-derived
factor in producing the broad range in color hues found in wild larvae.
The color-assessment techniques described here could be used to better
understand the role of color pattern in thermoregulation, sexual
selection and predation- avoidance.
Introduction
Body color is a universal life attribute that influences intraspecific
communication, predator avoidance, and/or thermoregulation. Syste-
matists use color patterns to characterize species and subspecies,
especially in avian and lepidopteran taxa. Despite these important roles,
color patterns are usually qualitatively described, not quantitatively
characterized. Partly, this is due to the difficulty in quantifying and
standardizing color description. Color standard texts (e.g., Munsell,
1963) are useful, but not widely accessible. Each text uses different
descriptors and their value is limited mainly to mono-colored organisms.
An added complexity is the variation in color pattern within popula¬
tions. This is particularly apparent in the Lepidoptera, with color
polymorphism occurring in LARVAE (e.g., Poulton, 1888; Bell & Scott,
1937; Pinhey, 1960; Clarke, Dickson & Sheppard, 1963; Curio, 1965,
institute of Ecology, University of Georgia, Athens, GA 30602
2Dept. Entomology, University of Georgia, Athens, GA 30602
25(3): 188-201,1986(87)
189
1970a, 1970b, 1970c; Boer, 1971; Emmel & Emmel, 1973; Common &
Waterhouse, 1981; see also Edmunds, 1974), PUPAE (Poulton, 1890;
Sims & Shapiro, 1983, and citations therein), and ADULTS (Ford, 1955;
Kettle well, 1961; Clarke & Sheppard, 1963, 1972; Owen & Chanter,
1969; and citations in Wickler, 1968 and Rettenmeyer, 1970). Larvae of
the federally endangered (U.S. Fish & Wildlife Service, 1976) San Bruno
elfin butterfly, Callophrys mossii bayensis R. W. Brown exhibit a
striking color polymorphism, with chromatic variability of both larvae
and foodplant substrates. This provides an ideal situation for comparing
color assessment techniques.
Callophyrs mossii bayensis Color Morphs
Brown (1969) first described color morphs in third and fourth instar C.
m. bayensis. He felt that greenish, fresh-hatched larvae acquired the
same color as the Sedum spathulifolium Hooker foodplant part they
ingested. Sedum exhibits diverse colors in late spring when larvae are
near maturity: Basal leaf rosettes range from deep green to rosy red.
Flowering stalk stems and bracts are initially green, becoming pale to
rosy, or deep red; petals are yellow.
Brown’s assessment of color determination was disputed by Emmel
and Ferris (1972), who described three distinct color morphs from
laboratory-reared fourth instars fed only green Sedum rosettes: yellow,
pale orange, and cherry red. Arnold (1978, 1983), in turn, disputed the
concept of three distinct morphs: “Newly eclosed larvae were colored
either red or yellow. They remained one color throughout their larval
life,” and “larvae possess two distinct color morphs, red and yellow, plus
an intermediate light orange.” Lumping light orange and yellow larvae,
Arnold proposed a simple 1:3 allelic expression of yellow:red forms, and
equated laboratory and field expression of larval color. Finally, our
repeated field observations of an array of color forms conflicts with all
previous reports of two or three distinct morphs in nature. Clearly, there
are discrepancies regarding the expression of color, its stability, and its
derivation in C. m. bayensis. This paper seeks to resolve some of them.
Materials and Methods
C. m. bayensis and Sedum spathulifolium samples were obtained on
north-facing slopes of San Bruno Mountain (San Mateo County) Califor¬
nia between Brisbane and Colma Canyon. Larvae occur from about
mid-March to very early June. About mid-May, third and fourth instar
larvae ascend to budding Sedum flower stalks (Emmel & Ferris, 1972;
Arnold, 1983). We took food-plant and fourth (penultimate) instar
samples after ascent.
COLOR CLASSIFICATION SCHEME: Following a preliminary 1977
field examination, a scheme was developed to quickly color-sort wild
larvae: Seven larval “standards” (Fig. 1) divided the visual color range of
190
J. Res. Lepid.
i
wild larvae. These were sequentially numbered; the higher the number,
the more red (or less yellow) the larva. These were photographed with
Kodachrome 25 film, using two Sunpak 411 flashes. Subsequent Kodak
color prints facilitated rapid color classification in the field. Although
film color reproduction is inexact, we found no problem placing wild
larvae into one of seven color categories. A “color category” represents a
range between two points defined by the larval standards, except for
Category 7 which had only one larval standard “anchor.” A larva whose
general color fell anywhere between the discrete point of Standard 1 up
to, but not matching Standard 2, was a Category 1 larva and so on.
COLORIMETER ANALYSIS: Live larval and foodplant samples were
color-analyzed using a Hunterlab Tristimulus Colorimeter Model
D25M-9. This employs a source-photodetector-filter combination to
simulate the colormatching response functions of a “normal” human
observer. Quantifiable, repeatable results are in the form of the Lx ax b1
(henceforth, LAB) system (Hunter, 1975). “L” measures brightness
(L = 100 for pure white, 0 for pure black). “A” and “B” are chromaticity
dimensions. The value of “A” indicates redness ( + value), gray (0 value),
and green (— value). “B” measures yellowness (+ value), gray (0 value)
and blue (— value). Measurements were made by holding similar-sized
samples of Sedum flowers and adjacent bracts, secondary bracts, green
rosettes, or C. m. bayensis penultimate instar larvae against the 1/2-inch
diameter port.
SPECTRAL ANALYSIS: A Cary UV-VIS spectrophotometer with spec¬
tral capacity of 187 — 875 nanometers (nm), and equipped with a diffuse
reflectance sphere, was used. Larval and foodplant samples were affixed
in similar orientation on coal black cards with double-stick tape. Each
sample was scanned at 1 nm/second, with a spectral band width of 3.5
nm, allowing resolution of narrow reflectance peaks. To reduce sample
orientation effects, all samples were positioned similarly. After scan¬
ning, larvae were released unharmed by wetting the double-stick tape.
LARVAL COLOR CHANGES: To explore short-term color changes,
fourth instar larvae with previous access to all Sedum plant parts were
segregated into color categories using the seven standards. Free access
to all foodplant parts was maintained under low intensity fluorescent
lighting. Forty-eight hours later, the larvae were color-reclassified. Only
tachinid parasitoid-free larvae (assayed at pupation) were used in the
data analysis.
We investigated Brown’s (1969) statement that larval and ingested
food colors converged: Larvae that had ingested only green rosettes for
two days were grouped into pairs of identically colored larvae and
color-classified. For the following 48 hours, one member of each pair was
provided only yellow Sedum flowers; the other was given only very red
flower stalk bracts. All experienced the same fluorescent light exposure.
Pairs then were reunited and color-compared, using the larval stan¬
dards. Only parasitoid-free larvae were used in the data analysis.
25(3): 188-201, 1986(87)
191
Fig. 1. Seven larval "standards" used to characterize color polymorphism in
wild Callophrys mossii bayensis. Standards are labeled sequentially,
starting with the most yellow (Top row, 1-4; bottom row, 5-7).
Fig. 7. (LEFT BELOW) Larval color shift from light to dark over a 48-hour period.
LEFT: Flower-fed larva now in color Category 3, formerly Category 2;
RIGHT: Red bract-fed larva, unchanged in Category 2.
Fig. 8. (RIGHT BELOW) Larval color shift from dark to light over a 48-hour period.
LEFT: Flower-fed larva now in color Category 5, formerly Category 6;
RIGHT: Red bract-fed larva unchanged in Category 6.
192
J. Res. Lepid.
i
Results
QUALITATIVE DESCRIPTION OF LARVAL COLOR: Nearly 500
wild larvae were color-classified. Virtually none were lighter yellow than
Standard 1; some had less pronounced “chevrons,” the paired, dorso¬
lateral curved markings occurring on many body segments. Category 7
proved exceptionally restrictive, since few Category 7 larvae were
redder than Standard 7.
Larvae within each color category can be generalized as follows:
1 = Yellow, no peach tint; chevron markings generally faint
2 = Yellowish with faint orange tint; distinct chevrons.
3 = Distinctly light orange with slightly darker rosy suffusions;
chevrons usually with pale outlines.
4 = Orange with darker peach-colored suffusions on much of the body;
chevron outlines and dorsal midline generally pale.
5 = Orange with brownish tinge; dark chevrons and less distinct pale
outlines.
6 = Rosy red, with less distinct but noticeable pale chevron outlines.
Larvae in this category may be lighter colored than the previous
category, but are distinctly redder.
7 = Cherry red throughout; chevrons generally faint.
While color category designation was based upon general background
color, ignoring fine-scale pattern differences, we also noted that chevron
markings did not intensify in direct relation to increasingly red back¬
ground coloration (see Emmel & Ferris, 1972).
COLOR DISTRIBUTION IN NATURE: Fig. 2 shows the color distribu¬
tion of 433 wild larvae, comparing the results to distributions obtained
by Emmel and Ferris (1972) for wild larvae, and Arnold (1978) for
laboratory-rearings. This alignment easily satisfied the “morph” de¬
scriptors provided by each author for his respective sample. Our
categories 2 and 3 are the only ones that would fit the definition of “light
orange” ( sensu Arnold, 1978).
Our sample indicates larvae to be broadly distributed across color
categories, at these frequencies: 1 = 6.0%; 2 = 10.6%; 3 = 14.6%;
4 = 13.9%; 5 = 12.0%; 6 = 24.7%; 7 = 18.3%. Further, our sample yielded
lower frequencies of “pure” yellow (Category 1) and red (Category 7 and
possibly 6) larvae than reported for laboratory rearings. Conversely,
greater frequencies of “intermediate” colors were found. Even when
restricting “intermediates” to larvae of categories 2-3, our combined
frequencies of yellow plus “light orange” larvae (over 30%) exceed that of
the laboratory-reared sample (24.4%; Arnold, 1978). Unfortunately,
Arnold did not segregate frequencies for yellow and light orange larvae.
Yet, he states that only “a few individuals are light orange” (Arnold,
1983), which tends to corroborate our observations of rosette-reared
larvae, and by deduction, confirms the much rarer occurrence of “pure
yellow” larvae in nature.
25(3): 188-201, 1986(87)
193
EEC
]
Fig. 2. Color category distribution of C. m. bayensis larvae: Comparisons of
wild- and laboratory-derived samples, from (A) Arnold, 1978; (B)
Emmel & Ferris, 1972; (C) this study. Alignments are based upon each
author's color descriptions of cited morphs. Frequency figures within
each bar pertain to that study. Above-barfrequencies in (B) and (C) are
provided to facilitate cross-sample comparisons.
COLORIMETER VALUE COMPARISONS: Table 1 lists LAB values
for C. m. bayensis larval standards and foodplant samples. Predictably,
“A” values are higher for the “redder” larval standards, although the
most yellow standard reflects some red. The “redness” increase, mea¬
sured by “A,” changes little for standards 2-5, increasing for 6 and 7. In
contrast, “yellowness,” measured by “B,” drops in significant increments
through standard 5. Thus, while larval standards broadly cover the
yellow-to-red spectrum, they do not represent evenly spaced color points
for either chromaticity dimension. This is clear in the composite express¬
ion of color (subtracting “A” from “B” for each sample; Table 1). These
findings, however, again confirm a graded expression of color in wild
larvae within their spectral range.
The range in larval LAB values approximates that of foodplant parts
(Table 1). However, pale or yellowish flowering stalk substrates
(flowers + associated racemes) exhibit significant green colorimeter
values (i.e., negative “A”) that are not duplicated in any larval standards
or in Category 1 larvae. In contrast, there is close matching of “A” and
“B” values for the reddest Sedum samples and larvae.
SPECTRAL VALUE COMPARISONS: Sample orientation (Fig. 3),
brightness, and other features of the sample can affect absolute reflect¬
ance values. However, basic reflectance peaks and dips are relatively
194
J. Res. Lepid.
Table 1 . LAB colorimeter values for Cal/ophryr mossii bayensis larval stan¬
dards and Sedum spathulifolium foodplant samples. Variation of
each sample did not exceed 10% between readings as long as
orientation positions were
kept constant.
Sample
Color Values
L A
B i
(B-A)
Larva: Color Standard 1
37.52 2.81
12.17
9.4
Color Standard 2
36.51 4.01
10.21
6.2
Color Standard 3
35.52 4.53
8.95
4.4
Color Standard 4
35.02 4.68
6.65
2.0
Color Standard 5
34.08 4.91
4.37
-0.5
Color Standard 6
34.30 6.83
3.98
-2.9
Color Standard 7
32.94 7.72
3.76
-4.0
Sedum Flowers: Sample 1
35.27 1.80
24.13
Sample 2
40.59 3.45
15.36
Sample 3
45.22 -2.05
19.70
Sample 4
40.55 .70
17.33
Sample 5
36.73 -1.74
18.22
Sedum Leaves: Sample 1
33.17 -6.03
13.01
(green) Sample 2
40.88 -6.82
12.42
Sample 3
47.21 -5.90
13.60
Sample 4
38.74 -2.85
5.59
Sedum Bracts: Sample 1
33.14 9.08
3.56
(reddish) Sample 2
28.23 6.27
3.55
Sample 3
35.41 4.33
4.97
Sample 4
38.10 7.44
3.34
Sample 5
44.20 4.97
2.19
Cumulative Spectral Ranges:
L A
B
Larvae .
32-37 2.8-
-7.7 3.8
-12.2
Foodplant Rosettes .
28-47 -6.0-
-9.1 2.2
-24.1
Flowering Stalk .
28-45 -2.1-
-9.1 2.2
-24.1
nanometers
Fig. 3. Reflectance spectra of a Sedum spathulifolium leaf sample placed at
different angles in the spectrophotometer diffuse reflectance sphere
sample port.
% reflectance
25(3): 188-201, 1986(87)
195
constant. For this reason, we limited our spectrograph comparisons to
reflectance curves (slopes).
In the ultraviolet and infrared (Fig. 3), no distinguishable intersample
differences were found. All samples reflected strongly in the red and
near-infrared range but weakly in the ultraviolet.
Figure 4 A shows reflectance curves for the larval color standards.
Predictably, Standard 1 (yellow) reflects highly between 600-630 nm,
while Standard 7 (red) exhibits a sharp reflectance drop at wave-lengths
under 640 nm. Reflectance differences are less pronounced for standards
that are closer in visual color. In Figure 4B, the curves are aligned at 550
nm to show relative similarities. Standards 4—7 reflect almost identical¬
ly below 550 nm. Standards 1—3 show similar reflectance patterns but
greater variation, especially Standard 1.
Regardless of visual appearance, S. spathulifolium samples (Fig. 5)
usually exhibited a broad absorbance peak (reflectance dip) at 670- 680
nm. Dry flower stalk stems (Fig. 5: ST) were the only exception. Larvae
that matched standards 1 and 7 were run sequentially with like-colored
Sedum parts (yellow blossoms or deep red flower head bracts (Fig. 6).
Visual colors are not backed by fine-scale spectral reflectance mimicry.
Most conspicuously, the foodplant reflectance dip at 670—680 nm is
absent. As seen in the colorimeter data, larval Standard 1 does not show
the strong yellow-green reflectance peak of the Sedum flower sample.
Moreover, while the slope of Standard 7 and its red Sedum counterpart
are very similar between 600—630 nm, at shorter wavelengths larvae
have relatively higher reflectance values. Possibly, these plant-caterpil¬
lar differences are partly derived from structural disparities.
COLOR SHIFTS IN INDIVIDUALS: Over one-third of larvae given free
access to foodplant parts changed color over a two-day period (Table
2); some changed within the first day. Color shifts occurred in larvae of
all color categories examined (1-5), with Category 4 a possible excep¬
tion. All but one (a shift from 5 to 3) of the 16 color shifts spanned one
category. As defined here, a larva “color shifts” by crossing at least one
color anchor (defined by a larval standard). However, twro larvae
experiencing the same “one category” change, in reality, may have
shifted significantly different amounts.
Table 3 summarizes color shifts of 34 color-matched pairs, after being
fed different-colored Sedum parts. Fifteen out of 68 larvae colordiverged
from their pair mates; two examples, in different spectral directions,
are illustrated in figures 7 and 8. As in the previous experiment, a
Fig. 4. Reflectance spectra of C. m. bayensis larvae. A: Scans from "most
yellow" (Standard 1 ) to "most red" (Standard 7) larvae in the 400-700
nm range; samples were of like size, so major differences in absolute
reflectance values between samples are valid. B: Realignment of the
seven larval standard scans at 550 nm show relative similarities of
curves.
400
nanometers
700L ^ \X VjnJ % reflectance
-*■ to (l/2)Ll
-
-
-
-
X
X
X
X
X
X
most
AB5 of antlers! 1/2 )L1
X
X
X
X
some
6. body pigmentation
lines and crenations only
X
X
X
X
X
-
-
-
-
-
most
additional longitudinal bands
-
-
-
-
-
X
X
X
X
X
some
7. feeding behavior
not gregarious as early instars
X
X
X
X
all?
gregarious as early instars
-
-
X
X
X
X
X
X
none?
PUPA:
8. thorax
metanotum >abdomen 1
X
X
X
X
X
X
X
X
-
-
most
metanotum0.7
X
X
X
X
some
v/ssO.7
-
-
-
-
X
X
-
X
X
X
most
20. valve/aedeagus (m)
v/a>0.65
_
X
X
X
some
v/a<0.45
X
X
many
GEOGRAPHIC RANGE:
western N. America
X
X
_
-
X
X
J
_
X
_
estern N. America
-
-
X
X
-
-
X
X
-
_
peninsular florida
-
-
X
X
-
-
-
X
-
-
Central America
X
-
Greater Antilles
X
longitudinal ribs of the eggs. The position of the aeropyles corresponds
with the ends of the ladder-like horizontal costulae found between the
ribs. Aeropyles are absent on the lower halves of the ribs only in the
Clyton group of Asterocampa.
3. The number of eggs in a clutch ranges from 1 (deposited singly) to
well over 500 in a mass for hackberry butterflies. Not many butterflies,
and few apaturines, deposit their eggs in distinct clusters consisting of
hundreds of eggs. The most space-saving packing design for spherical
units such as these eggs approximate is tetrahedral. The behavior
necessary for stacking eggs in such a uniform design is more complex
than that necessary to place eggs more randomly, whether in piles or
25(4): 215-337, 1987(88)
285
singly. Even though members of some populations of the Celtis group of
Asterocampa are known to deposit fairly large clutches, the eggs are not
strictly tetrahedrally packed as they are in masses deposited by females
in the Clyton group. There are few reports of egg depositing behavior in
other Apaturinae.
A character correlated with large clutch size is oviposition on mature
(old) leaves. This character sate is tentatively considered a derived
character state. From the viewpoint of leaf toughness new leaves are
both thinner and less tough than old leaves, providing more suitable
food for early instar larvae. Chemistry (toxins, deterrents) and nutri¬
tion obviously enter into the determination of host suitability. New
leaves were found to sustain maximal growth of all hackberry butterfly
species in early instars so that there would appear to be no outstanding
palatability problem in Celtis other than toughness. Early instar larvae
of the Clyton group feed gregariously on old leaves and so appear to have
made this great food resource available, whereas single larvae are
apparently unable to sustain growth on old leaves (personal observa¬
tions on larvae of both A. clyton and A. celtis ). However, there could be a
complicating factor to the interpretation that individual larvae are
unable to sustain growth on old leaves if behavioral problems arise due
to isolation of a gregarious feeder from external cues from its normal
feeding partners (Kalin and Knerer, 1977). It is also possible that
placement of the eggs on old leaves away from the tips of branches is a
means of avoiding egg parasites, which is especially important when
virtually all the eggs of a single female are in one place. Female choice of
mature trees only as suitable oviposition sites is viewed as a behavioral
restriction. Clyton group females generally do not place eggs on juvenile
or small trees in spite of apparently suitable food being there.
4. Neotropical Celtis , subgenus Momisia, is thought to be colo¬
nizing northward into the ranges of hackberry butterflies. There are
both structural and chemical differences between Nearctic and Neotro¬
pical hackberries. Subsequent adaptation by some populations of but¬
terflies for usage of these plants as larval hosts is considered to have been
a major evolutionary step in the evolution of Asterocampa. A. leilia has
specialized on one species of Neotropical hackberry, Celtis ( Momisia )
pallida , and has at present not been successfully reared on any other
species of hackberry. The phylogeny of Celtis worldwide has not been
hypothesized. Most other Apaturinae feed as larvae on species of Celtis.
5. The lateral scolus AB5 of the antlers extends the lateral frill of head
scoli up onto the antlers. This condition is not found in the Celtis group
of Asterocampa , where AB5 is rather short or vestigial, separating the
antlers from the lateral frills. The reduction of scoli on the antlers
enhances crypsis and is tentatively considered to be a derived condition.
If true this condition is an easily achieved autapomorphy and might
well have occurred many times within the Apaturinae.
Antler length is also involved. Short antlers are rarely found among
286
J.Res.Lepid.
apaturine nymphalids. Stouter, shorter antlers are found in the Clyton
group of Asterocampa. This condition is viewed as a possible adaptation
to gregarious behavior.
6. Asterocampa larvae are typically cryptic in coloration. They are
green with lines and crenations of whitish yellow. In addition, larvae of
the Clyton group develop longitudinal bands of whitish yellow pig¬
mentation under the cuticle, a condition not known to me to be found in
many other apaturines. This suite of markings produces a disruptive
appearance rather than crypsis and might even be a mimetic or
aposematic signal to some unknown predator observer.
Crypsis in enhanced in other populations of hackberry butterflies by
the reduction of all light-colored body markings of the larvae. This
condition appears independently within the genus.
7. No other apaturine larvae have been reported to be gregarious
feeders other than those of the Clyton group of Asterocampa. Gregarious
hackberry butterfly larvae communicate by silk trails and touch (pers.
obs.). They exhibit a feeding site cleaning behavior, active frass removal,
which is considered to be a defense against potential predators and
parasites which might locate the larvae by the volatile chemicals in the
frass. Caterpillars have been observed to bite pellets of frass and throw
them off leaves on which the larvae are feeding.
8. Apaturine pupae are not typically highly arched or irregular in
outline but this condition occurs in a few genera. The pupae of Astero¬
campa idyja are slightly more arched than those of other members of the
genus. A measure of this arching is the relative length of the metano-
tum to that of the first abdominal segment.
9. The abdominal keel is composed of the dorsal ridge of abdominal
segments 3-8. Anteriorly these segments are either pointed (Clyton
group) or blunt (Celtis group).
10. The morphology of the cremaster in most apaturine pupae is
typically nymphaloid in appearance. A few Apaturinae have a greatly
elongated cremaster which serves to hold the pupa flush against its
substrate. Asterocampa and Chitoria are the only genera to accomplish
this by a highly elongate pad of hooks reaching anteriorly to the level of
the sustainers. Within the hackberry butterflies only A. leilia does not
have an elongate bed of cremastral hooks. The anterior area normally
occupied by the cremastral hooks is replaced with short, undifferentiated
setae. This condition is viewed as a modification by loss or de-differenti¬
ation, rather than a primitive condition.
11. Most apaturine butterflies have the bars in the discal cell
unbroken; that is, there are only 2 bars, one somewhat centrally placed
and the other placed at the end of the cell. In some Apaturinae the more
basal bar is “broken” into 2 spots, the anterior half of the bar a greater or
lesser distance from the origin than the posterior half. The halves
evidently lie in different fields by reason of their belonging on different
sides of the median vein during development of the discal cell. Only
25(4): 215-337, 1987(88)
287
Asterocampa celtis has a broken discal bar among the hackberry
butterflies.
12. The zigzag pattern of postmedian spots found in most hackberry
butterflies might be ancestral in Asterocampa. Only A. idyja has
postmedian spot M2 adjacent to M3, the postmedian spots more or less
form a linear band on the forewings. All the anterior foci are more basal,
resulting in the correlated character of the discal bars placed very close
together. It is possible that this modification was brought about by
selection favoring a phenotype closer to the pattern of other sympatric
subtropical butterflies. The latter might serve as models within a
mimicry ring. Smyrna blomfildia (Fabr.) is one such butterfly with a
pattern very much like that of A. idyja. It is a very strong flier and might
serve as a model for the weaker-flighted hackberry butterfly. The
relative palatabilities of these butterflies has not been tested. In the
light and typical phase of A. idyja argus the band on the fore wings is
further modified into a thicker, solid golden band. This phenotype is
even more like that of Smyrna.
Virtually all Apaturinae do not show this zigzag pattern and have
postmedian spots M2 and M3 equidistant from the base of the wing. In
some species, M2 is even more basal. I do not feel that out-group
comparison would lead one to the right hypothesis of polarity for this
character.
13-15. Various apparent reductions and other modifications of limbal
spots in the FW can be considered derivations of a basic nymphaloid
ground-plan with well-formed eyespots. Clyton group hackberry but¬
terflies have lost all eyespot expression in the fore wings.
I can’t help but feel that the common denominator, or primitive
condition, in the Apaturinae is to have only limbal spot Cul expressed
as an eyespot. Could spots Ml and M3 become derepressed in A. leilia
and A. celtis antonid ? The genetics of pattern formation in hackberry
butterflies would be an interesting and enlightening study.
16. The expression of limbal spot A2 as an eyespot in the HW as
considered relative to the basic nymphaloid plan is primitive. It is not
found at all in the Clyton group of Asterocampa , nor, to my knowledge,
in any other Apaturinae, except members of the Celtis group.
Could hackberry butterflies be specializing evolutionarily in a form of
predator avoidance as adults by derepression of eyespots, rather than by
disruptive coloration (or some other such tactic)?
17. A brush of hair-scales is found dorsally on the membrane separat¬
ing the male genitalia and the eighth abdominal tergite in hackberry
butterflies. These are erected when the genitalia are extruded. This
brush is found in many apaturine butterflies. The hair-scales are
straight or curved in Asterocampa , but are usually straight in other
Apaturinae. The anal brush of the male terminalia would appear to be
apomorphic in the recurved condition (A. celtis ).
18. The uncus in male Apaturinae is almost always pointed poster-
288
J.Res.Lepid.
iorly. A few species have a bifid uncus with a narrow notch. All
Asterocampa have a bifid uncus, but the notch is very shallow and the
points very blunt in Celtis group members.
19, 20. Most apaturine butterflies (all genera have been examined)
have fairly long male genitalia (lengths of saccus and aedeagus relative
to length of valves). The ductus bursae of the female is similarly
elongated in these butterflies. In some Apaturinae the valves are
secondarily quite long (e.g., Sasakia). In Asterocampa , members of the
Celtis group have relatively shorter aedeagi and sacci relative to valvi
than do members of the Clyton group. Measures of these lengths can be
expressed in terms of ratios of lengths. These ratios can serve to
separate species of hackberry butterflies. It is not known whether or not
these differences might serve as mechanical isolating factors.
The ability of different populations to interbreed is a species char¬
acteristic. Speciation may occur without this ability being impaired if
some other genetically isolating mechanism is evolved. Therefore, the
ability of populations to interbreed is viewed as a symplesiomorphy and,
correspondingly, the inability to interbreed is a possible synapomorphy.
Field and laboratory studies indicate lack of interbreeding between
most species pairs of hackberry butterflies, but it is not known whether
Asterocampa idyja can interbreed with A. clyton. Other pairings of A.
idyja would most probably be negative.
One adult character left out of the table is color phase expression. All
species of hackberry butterflies have the ability through an unknown
genetically mediated mechanism to express both a light and dark
phenotype. The expression is carried out through what appears to be a
low or high number of wing and body scales attaining darker pigmenta¬
tion. Although the pathway of pigments has not been worked out in
Asterocampa , there is reason to believe that non-structural pigmenta¬
tion is mainly due to different or different oxidation states of [phaeo-]
melanins in the wing scales, much as it appears to be in the nymphalid
Precis coenia (= Junonia coenia (Hiibner)) (Nijhout, 1980b). In A.
clyton the dark phase has been given many names (e.g., “proserpina”).
Dr. W. J. Reinthal recognized phases in A. celtis (ms.), and spring A.
leilia are lighter than fall specimens. In some populations of hackberry
butterflies one or the other phase seems to have been lost (see: A. idyja).
Biogeographic characters are included in the table as a comparative
data set and will be discussed in the appropriate section. The pattern
given here seems to reflect the morphological character distribution but
other scenarios will be explored.
Wagner network analysis (Lundberg, 1972) revealed the existence of
both the Celtis and Clyton groups of hackberry butterflies (Table 9:
characters 1-3, 5, 7, 9, 14, 16, 18, 19) (Figure 8, Table 10). Other
character patterns confirm species differences (characters 8, 10-12, 17,
20 (both parts)). Character 4 is better interpreted as a homoplasy for
host plant use between A. leilia and one population of A. celtis antonia.
25(4): 215-337, 1987(88)
289
Characters 6, 13, and 15 involve pigmentation and show convergences
in states among the species. The characters 4, 6, 13, and 15 were coded
accordingly for network analysis.
Table 10. Hackberry butterfly species distance matrix (Manhattan
distances as computed from Table 9).
TAXA LEILIA CELTIS CLYTON IDYJA HTU1 HTU2 “ANCESTOR”
LEILIA
-
-
-
-
-
-
-
CELTIS
5
-
-
-
-
-
-
CLYTON
15
16
-
-
-
-
-
IDYJA
18
19
3
-
-
-
-
HTU1
2
3
13
16
-
-
-
HTU2
15
16
0
3
13
-
-
“ANCESTOR”
4
5
11
14
2
11
—
HTU1 (with character states: 011101110111100111100) connects A.
celtis (011101110101100101110) to the interval between A. leilia
(011001110011100111100) and A. idyja (100110001110011010001).
HTU2 (100110011111011010000) connects A. clyton (10011001111101-
1010000) to the interval between HTU1 and A. idyja.
A hypothetical ancestor (111101110111100111000) was fitted to the
network, and it roots onto the interval between HTU1 and HTU2. The
resulting Wagner tree is shown in Figure 9.
Hypothesizing polarities for the characters one can postulate synapo-
morphies with which to construct a cladogram. A cladogram of rela¬
tionships among the 10 taxa of Asterocampa recognized in this revision
is shown in Figure 10. The relationships between taxa are presented as
a series of branching points where each furcation marks the postulated
origin of monophyletic taxa. The branching pattern is documented by
CELTIS
Fig. 8. Wagner network of hackberry species. Potential homoplastic characters
are in parentheses.
290
J.Res.Lepid.
hypothesized synapomorphies. The numbers on the cladogram corre¬
spond to those listed following the figure where argumentation for the
branching pattern is given.
Wagner calculations were made on the four species of hackberry
butterflies. The Wagner Network and Tree are congruent with the
proposed cladogram. Additional intraspecific taxa are attached within
the cladogram and discussed in the text.
The overwhelming conclusion one can draw from these dendrograms
is that the Celtis group and Clyton group of hackberry butterflies are
quite different from one another. The Clyton group is very well
supported by characters, the Celtis group less so.
Another observation is that Asterocampa clyton is poorly defined by
the characters examined in relation to A. idyja.
1 . The out-group used in the cladogram of hackberry butterflies is all
of the other apaturine genera. The possibility that Chitoria and Astero¬
campa are sister groups has been discussed. These 2 genera share the
presumably synapomorphic characters: 1) larvae with reduced basal
antler socli; 2) pupae with elongated cremastral pad; 3) male genitalia
with reduced gnathos. Whether Chitoria is a monophyletic genus or not
awaits investigation, as only the immature stages of one species, C.
ulupi (Doherty), are known. Asterocampa is considered to be a monophy¬
letic group. Members of this genus share the synapomorphy, male
genitalia with bilobed uncus, and all are Nearctic in distribution.
2. The Celtis group is thought to be a monophyletic group. The true
hackberry butterflies (proposed common name) share the following
IDYJA
"ANCESTOR*'
Fig. 9. Wagner tree of hackberry butterfly species.
25(4): 215-337, 1987(88)
291
Fig. 10. Cladogram of relationships among the hackberry butterflies in relation to
other Apaturinae.
probable synapomorphies: 1) eggs with wrinkled chorion between longi¬
tudinal ribs; 2) male genitalia with relatively short saccus; 3) reduction
of basal antler scolus AB5. These butterflies are relatively unmodified
from the hypothetical archetype, the adults having virtually all of the
limbal eyespots well developed on both surfaces of both wings.
The Clyton group is the monophyletic sister group of the Celtis group
of hackberry butterflies. These are distinguished by the synapomor¬
phies: 1) eggs lacking aeropyles on lower (bottom) halves; 2) eggs
deposited in tightly packed multi-layered masses; 3) larvae gregarious
as early instars; 4) larvae banded; 5) adults with virtually all limbal
spots in FWs not expressed as dark spots; 6) limbal spot on anal cup
ventrally not expressed (HW limbal spots ventrally generally not well
expressed). Other characters used to distinguish the Clyton group
include: 1) segments of pupal abdominal keel anteriorly sharp; 2) male
genitalia with narrowly notched uncus. This is a well-defined taxon for
which the common name of American emperors is proposed.
3. Asterocampa celtis and A. leilia appear to be sister species. The 3
recognized subspecies of A. celtis share the following synapomorphies:
1) they have apparently lost the ability to interbreed with A. leilia (only
A. celtis antonia tested in laboratory breeding trials); 2) the basal discal
bar is divided into 2 spots (broken discal bar); 3) the male brush over the
terminalia is recurved. A. leilia has the following autapomorphies: 1)
sole usage of Celtis pallida as larval food plant; 2) pupal cremastral bed
292
J. Res. Lepid.
of hooks shortened so that pupa does not hang flush against its retaining
surface; 3) female genitalia with very short ductus bursae; 4) high
temperature tolerance in all life stages.
4. The 2 more eastern subspecies of A. celtis are distinguishable from
A. celtis antonia by the reduction of expression of FW limbal spots M3
and Cul. Unlike A. celtis celtis and A. celtis reinthali, A. celtis antonia ,
in one of its populations (called here “mexicana”), uses Celtis pallida as
a larval food plant.
5. A. celtis celtis and A. celtis reinthali are sister subspecies (if there
are such things). This eastern United States clade is distinguished by
the synapomorphies: 1) virtual loss of basal antler scolus AB5 in larvae;
2) lack of expression of limbal spot M3 in FWs of adults. The latter
subspecies is distinguished by: 1) large size; 2) found in peninsular
Florida; 3) limbal eyespot Ml of HW asymmetrically drawn out into
point; 4) pupil of limbal eyespot Cul of FW lateralized. The latter 2
characters might well be correlates of large adult body size.
6. Asterocampa clyton and A. idyja are sister species. A. clyton is
characterized by its presumed inability (virtually allopatric) to inter¬
breed with A. idyja , but otherwise retains the hypothetical primitive
character set of the Clyton group. Asterocampa idyja has the autoapo-
morphies: 1) larva with darkly pigmented anal horns (not always
expressed); 2) pupa with relatively short metanotum as measured
dorsolongitudinally; 3) postmedian spots in anterior portion of the wing
closer to discal cell than in other hackberry butterflies. It is also
characterized by having a relatively long aedeagus and saccus in the
male (genitalia).
7. The 2 more eastern subspecies of A. clyton are more similar to each
other than either is to either of the 2 more western subspecies, based on
pigmentation of larvae and adults. The antlers of caterpillars of A.
clyton clyton and A. clyton flora are relatively shorter than those of A.
clyton texana and A. clyton louisa. FW limbal spot Cul is virtually never
even partially expressed in the 2 more eastern subspecies.
8. A. clyton texana and A. clyton louisa are presumably sister
subspecies. These subspecies have no readily apparent synapomorphies,
but A. clyton louisa has many character differences from A. clyton
texana (= “subpallida”), the polarities of which are unknown (e.g.,
larval and adult pigmentation, geographic range). A. clyton louisa
inhabits the same geographic area as A. celtis antonia form “mexicana.”
9. A. clyton clyton and A. clyton flora are sister subspecies, just as A.
celtis celtis and A. celtis reinthali are, respectively. A. clyton flora is
characterized by: 1) large size; 2) found in peninsular Florida; 3)
virtually lacking individuals expressing dark phase phenotypes.
10. Asterocampa idyja is composed of 2 phenotypically rather dif¬
ferent subspecies. The nominate subspecies is found in the Greater
Antilles, a geographic character considered here to be autapomorphic.
A. idyja argus has a banded form which is involved in a Neotropical
25(4): 215-337, 1987(88)
293
mimicry complex. The unbanded form is quite similar to A. idyja idyja ,
but is not nearly as pale.
It is informed conjecture to say that A sterocampa leilia speciated from
the A. celtis line by largely allopatric adaptation to its present host
plant. The ancestral A. celtis , remaining on the tree-like hosts like all
the other hackberry butterflies, would then lose the solid basal discal
bar in the wings for some obscure reason. It is interesting to note that
the phenotypically primitive A. celtis antonia (form “mexicana”) uses
Celtis pallida as a larval host together with the tree-like hackberry
species. Perhaps colonization of spiny hackberry represents a space into
which A. celtis populations can speciate.
In the opinion of this author, the inclusion of A. leilia with A. celtis to
form a species group is justified on phenotypic and ecological grounds,
although it is not well supported by cladistic argumentation.
The problem with hypothesizing a clade for taxa below the species
level is that there is presumably the ability of such taxa to exchange
genetic information with conspecifics, thus affecting the relative
“possession” of apomorphic characters. Characters are often main¬
tained as polymorphisms in such populations and rarely become fixed.
With such possibilities of interchange even fixed characters are liable to
become polymorphic again. For these reasons taxonomy based strictly
on clades below the species level should be done cautiously if at all (see
also: Baum and Estabrook, 1978). Such clades as are presented here rest
largely on the improbability of genetic exchange between largely
allopatric populations containing relatively sedentary individuals.
Classification based on these clades freezes this moment in their
evolutionary time. It is not unreasonable to suppose that both Floridian
subspecies of A. celtis and A. clyton, respectively, will gradually inter¬
grade with and merge into their respective nominate subspecies,
barring a near future re-isolation.
BIOGEOGRAPHY:
The distribution of hackberry butterflies can be given evolutionary
explanation with the application of techniques of historical biogeo¬
graphy (Cracraft, 1975). Before the emergence of vicariance bio¬
geography as an acceptable explanation for distributions of some
organisms, continental drift was a source of controversy with regard to
butterflies of North America (Eliot, 1946; Forbes, 1947). North America
does not seem to have an endemic family to butterflies, unless it is the
Papilionidae (Hancock, 1983). All the New World family-level groups
can theoretically be derived from ancestral Old World forms (Smart,
1979) via the Bering Strait or West African/Eastern South American
connections existing before the total break-up of Gondwanaland. The
few relict groups (recognized as such) of butterflies in the New World are
confined to mountains and islands.
The distribution of temperate and subtropical Nearctic butterflies has
294
J.Res.Lepid.
been a source for biogeographic speculation, often without the aid of
scientific methodology, which has given rise to a few precepts:
1. Glacial maxima with coordinate changes in American climate and
vegetation zones (Delcourt and Delcourt, 1981) must have pushed
butterflies into refugia (Brown, 1981; Klots, 1965). Recolonization of
temperate North America is occurring today, at different rates for
different butterflies. This colonization includes butterflies mostly of
Neotropical origin.
2. Only certain butterfly groups have widely dispersing females that
are good enough colonists to cross mountain or water barriers. To
account for the wide distribution of other butterflies, their females must
have had easier routes of colonization, either by land- (or host plant-)
bridge or by land connection of close proximity which no longer exist
today (vicariance is highly probable for some).
3. Isolation and allopatric speciation account for most of the taxono¬
mic diversity observed in butterflies. Subsequent sympatry of closely
related butterflies is a recent event owing to changes in climate, habitat
and distribution of host plants.
Looking again at the cladogram generated for hackberry butterflies
and replacing the taxa with the geographic areas they inhabit (Figs. 11,
12), there are patterns of distribution that could be assigned to either
dispersal or, alternatively, vicariance events. These patterns are dis¬
cussed by number, corresponding with the clades in the first figure.
1. The first noticeable feature of the graph is that Asterocampa is
found in North and Central America but is most closely related to Old
World genera, specifically to Chitoria which inhabits eastern Asia (ne.
India, se. Asia, central China, Formosa). What little there is known
about such a pattern of distribution would indicate that the most
attractive explanation for the New World location of hackberry butter¬
flies is a warm-climate, pre-Miocene (Arcto-Tertiary) dispersal of but¬
terflies from eastern Asia to North America by way of the Bering Land
Bridge. Subsequent isolation and adaptation may have given rise to
Asterocampa.
There are a few tenuous lines of evidence that strengthen the
argument for such an occurrence. The first question that might be asked
concerning the probability of Asterocampa also having been part of an
Arcto-Tertiary exchange is: Is there evidence of a continental inter¬
change of other organisms and, if so, when did it or they occur?
Looking at the present distribution of organisms there are many
species- and genus-level taxa that are found only in eastern Asia and in
similar climates in North America. An example would be plant
members of the Notophyllous Broad-leaved Evergreen forest (Wolfe,
1979), such as Liquidambar. The gall- and lerp-forming psyllids of the
genus Pachypsylla (also associated with Celtis) are among the insect
examples. They are distributed on hackberry in both North America
and in Japan (Hodkinson, 1980).
25(4): 215-337, 1987(88) 295
Fig. 11. Area cladogram of relationships among the hackberry butterflies in
relation to other Apaturinae.
Ifi >h
"h
□
Fig. 12. Flypothesized biogeographical
patterns shown by current
distributions of hackberry
butterflies.
T
296
J.Res.Lepid.
Land connections permitting such biotic transfers occurred many
times during the Tertiary (Hopkins, 1959). The Eocene/Oligocene is
theoretically more attractive than the Miocene for the interchange of
subtropical to temperate terrestrial organisms based on the climatic
inferences of the floristic evidence (Wolfe and Leopold, 1967). The latter
time period was evidently too cold to support appropriate flora. The
Middle Eocene flora from the Gulf of Alaska contains members of the
Ulmaceae having drip tips on their leaves (Wolfe, 1977) such as those
which are found on leaves in present day tropical forests.
2. The primary division in the genus Asterocampa is one of oviposition
strategy /host plant utilization and probably is not geographic. Females
of the Clyton group deposit large clutches of eggs on the host and the
early instar larvae feed gregariously. Oviposition is largely confined to
mature trees with large leaves and while the larvae grow better on new
growth of the host plant. They are able by eating together to consume
old growth as well. These butterflies are more often found in old stands
of their host plants which normally occur along rivers than those of the
other species group.
Females of the Celtis group deposit small numbers of eggs on their
hosts and the larvae feed more or less singly. Only new growth of the
host is available to early instar larvae even in A. leilia which has first
instar larvae with very well developed mandibles. Oviposition occurs on
the growing points of hosts usually on seedlings or the lower branches of
young trees. Oviposition in A. leilia is on the growing points of the host
bushes. Perhaps as a consequence of being more tissue specific (con¬
fined?), these butterflies are better colonists of their hosts and are wider
ranging. They are not only confined to river systems, but are also able to
find isolated stands of the host plant, much as the snout butterflies
(Libytheidae: Libytheana) do. Snout butterflies also feed on the new
growth of hackberry.
The 2 species groups occupy roughly the same geographic areas, with
the exception of the expansion southeastward of the A. idyja into the
Neotropics (6). It is a common occurrence to find one member of each
species group in a given locality and thus the various forms occur in
geographic pairs (e.g., A. c. antonia and A. c. texana + A. c. louisa, A. c.
reinthali and A. c. flora).
3. A. leilia appears to have invaded the more arid habitat of its host
permitting the butterfly to occur at lower local elevations and over
broader areas than the other grossly sympatric hackberry butterflies in
southwestern North America.
4 and 7. The A. celtis and A. clyton lines seem to have expanded
eastward leaving A. c. reinthali and A. c. flora as Pleistocene relicts in
peninsular Florida (5 and 9). Some differentiation of A. c. antonia has
occurred in northeastern Mexico where the females are smaller than
average and have decreased expression of FW limbal spots (form
“mexicana”). In this same area A. clyton texana has apparently differ-
25(4): 215-337, 1987(88)
297
entiated into A. clyton louisa which has darkened antennae and FW
apices (8).
10. The distribution of A. idyja is particularly interesting: one
subspecies occurs in the Greater Antilles and the other in Central
America. Its Caribbean host plant occurs in Central America as well. It
appears to be the lesser complicated explanation that the island
populations are derived from the mainland. The closest relative of A.
idyja occurs in the southwestern parts of North America adjacent to the
present distribution of A. idyja argus.
There are a number of hypotheses relating the major Caribbean
islands and organisms to Central America (Alain, 1958; Baie, 1970;
Comstock and Huntington, 1949; Freeland and Dietz, 1971; Khudoleg
and Meyerhoff, 1971; Pregill, 1981; Rosen, 1975; Scott, 1972; Shields
and Dvorak, 1979; Trelease, 1918). The first and most often cited
hypothesis holds that migrant females colonized the islands from the
mainland at a time when the configuration of land masses was as it is
now (large scale dispersal). Related hypotheses are similar but include
either a different configuration of land masses or, through sea level
changes, differing boundaries to existing land masses (short scale
dispersal and/or vicariance). The difficulties in differentiating between
vicariance and dispersal events are virtually insurmountable if both are
equally likely in the ignorance of the timing of such events (see also:
Howden, 1974). An extreme hypothesis (large scale vicariance) would
envision a single land mass inhabited by A. idyja which subsequently
split into 2 regions of which one is contiguous or equivalent to Central
America and the other to the Greater Antilles.
Because A . idyja is a relatively poor colonist I do not favor large scale
dispersal as the most likely event leading to its colonization of the
Greater Antilles. It also seems unlikely that the species is old enough
(stasis would have to characterize the evolution of morphological
characters in this species!) to have participated in a large scale vicari¬
ance event even if one did occur (Pregill, 1981). A short dispersal from
the Yucatan peninsula at a time when Cuba was effectively closer to
that part of Mexico is to me the most likely way in which A. idyja got to
the islands. This could have been achieved when a drop in sea level
occurred.
The timing of this hypothetical event is another matter. There is no
morphological evidence which might support early versus late dispersal
or vice versa. The island subspecies does not exhibit the presumed
mimetic morph (light phase individuals). This could be due to a founder
effect, a result of sampling fixation of a pre-existing polymorphism, or
just owing to the morph occurring at such a low frequency that it has not
yet been collected. This low frequency might be attributable to a lower
relative fitness of the mimetic morph in the island environment without
its presumed model (and selection agent?) being present.
The possibility of A. celtis occurring in Cuba (Lucas, 1857) is intri-
298
J. Res. Lepid.
guing. This species, with its better dispersal capabilities than members
of the Clyton group, would more likely be a colonist from Florida than
Central America. The probability of a form occurring in the Greater
Antilles being related to the Floridian A. celtis reinthali is therefore
higher, I think, than this from being related to A. celtis antonia. If this
theoretical butterfly were related to the latter, one would have support
for a generalized track for hackberry butterflies from Central America
to the Greater Antilles.
Figure 13 is given as a summary of hypothesized events in the
evolution of Asterocampa.
Conclusions
Asterocampa Rober is better known as a result of this revision. This
work has advanced the understanding of hackberry butterflies with
regard to their taxonomic history, morphological and behavior charac¬
teristics, and relationships one to another and to other apaturine
nymphaloid butterflies.
The application of Fabrician names to hackberry butterflies is ter¬
minated. Asterocampa celtis reinthali is described from peninsular
Florida because this butterfly population is distinct from A. alicia , here
considered a subjective synonym of A. celtis celtis. Three other taxa,
Asterocampa montis,A. leilia codes , and A. subpallida are synonymized
with A. celtis antonia , A. leilia , and A. clyton texana , respectively. Ten
different populations of hackberry butterflies are considered worthy of
valid names at this time.
Four species groupings were hypothesized after observation of but¬
terflies in the field and in trial breeding experiments in the laboratory.
These observations were supported by zoogeographic (Bowden, 1976)
and morphological differences in virtually all life stages observed. The
assignment of many taxa to subspecific rank represents a reduction in
rank from the classification of Miller and Brown (1983).
Fig. 13. Hypothesized Evolution in Asterocampa.
25(4): 215-337, 1987(88)
299
A table is presented which summarizes hackberry butterfly classifi¬
cation proposed in this revision (Table 11).
One population of hackberry butterflies was identified as being
characterizable but not considered worthy of subspecific status. This
population is designated as form “mexicana” of A. celtis antonia. It
occurs in the lower Rio Grande Valley of Texas and in northeastern
Mexico and is largely sympatric with A. clyton louisa.
Asterocampa is considered to be completely host specific on hackberry
{Celtis). A. leilia is host specific on Celtis pallida. Other species use a
variety of other species of hackberry as larval host plants, but only
exceptionally do they use C. pallida (one population of A. celtis antonia).
Table 11. Summary classification of hackberry butterflies and sug¬
gested common names.
Asterocampa Hackberry Butterflies
[Celtis group] true Hackberry Butterflies
1. celtis
[the] Hackberry Butterfly
a. celtis
[Eastern] Hackberry Butterfly
b. reinthali
Florida Hackberry Butterfly
c. antonia
Western Hackberry Butterfly
2. leilia
Desert Hackberry Butterfly
[Clyton group]
American Emperor Butterflies
3. clyton
Tawny Emperor
a. clyton
Tawny Emperor
b. flora
Florida Emperor
c. texana
Pale Emperor
d. louisa
[Rio Grande] Valley Emperor
4. idyja
Dusky Emperor
a. idyja
Dusky Emperor
b. argus
Banded Emperor
Keys and descriptions of all these taxa are presented in this revision.
Biological characteristics of each species are discussed. Distribution
maps and illustrations of all adult and most immature stages are given
in plates. Developmental studies of wing pattern development are still
needed to support suggestions of adult morphological evolution made
here. The ability to describe wing pattern and color in terms of
developmental foci and fields was very useful.
Cladistic methodology was used to hypothesize phylogenetic relation¬
ships among members of the genus Asterocampa and closely related
genera. Asterocampa is considered to share a recent common ancestry
with the eastern Palearctic genus Chitoria.
Two distinct groupings of hackberry butterflies emerged, based
on synapomorphic characters associated with 2 different life history
300
J. Res. Lepid.
strategies found in the genus. These were assigned species group status,
until the monophyly of the Celtis group is better analyzed.
Asterocampa is found to be Nearctic in distribution. Doxocopa , which
is a Neotropical genus with some members in North America, is quite
different from Asterocampa morphologically. It probably had a different
route of introduction into the New World than is proposed for Astero¬
campa.
Biogeographical interpretation of the phylogenetic pattern for hack-
berry butterflies developed through cladistic methodology yielded
several hypotheses. Populations of hackberry butterflies in the eastern
United States are seen to be derived from those of the Southwest. A.
celtis reinthali and A. clyton flora were thought to have evolved through
recent (not remote past) isolation in peninsular Florida. A. idyja idyja’s
arrival in the Greater Antilles is hypothesized to be from a population of
butterflies occurring in Central America at a time when such dispersal
would have been much more favorable than it is today. It probably was
also a fairly recent event.
The number of characters necessary by cladistic methodology to track
recent evolution in the genus were not found, leaving classification
below the species level unresolved by this method.
Traditional application of the biological species concept in conjunc¬
tion with studies of interpopulation sympatry and morphological char¬
acter state distribution helped in making decisions of which populations
should be accorded subspecific and which specific status. There are still
problems with classification at this level within the genus. These might
better be addressed through quantitative genetics studies.
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Plate 1 . Geographic distribution of Asterocampa celtis: • A. celtis celtis, I A.
celtis, • A ce/f/s reinthali, ) >4 ce/f/'s antonia.
Plate 2. Geographic distribution of Asterocampa leilia.
316
J. Res. Lepid.
Plate 3. Geographic distribution of Asterocampa clyton: • A. clyton clyton, i A.
clyton flora, I A. clyton texana, * A. clyton louisa.
Plate 4. Geographic distribution of Asterocampa idyja: A. idyja idyja, A. idyja
argus.
25(4): 215-337, 1987(88)
317
Plate 5. A. celtis celtis: A) E (top), Ontario, Canada; B) E (side, detail; C) E
(micropyle). A. celtis antonia: D) LI (top, head-note unbranched setae),
TX; E) LI (right side); F) LI (bottom, proleg-note crampets).
e = Egg
L1-L5 = First - Fifth Instar Larvae
P = Pupa
318
J.Res.Lepid.
Plate 6. A. celtis antonia: A) E (top), AZ; B) E (side), TX; C) E (side, detail), TX; D)
E (micropyle), TX.
25(4): 215-337, 1987(88)
319
Plate 7. A. celtis antonia: A) L5 (front, left part of head capsule), TX; B) L5 (side,
right part); C) L5 (back, left part).
320
J. Res. Lepid.
Plate 8. A leilia: A) E (top), AZ; B) E (micropylar region); C) E (side, detail); D) E
(micropyle).
25(4): 215-337, 1987(88)
321
Plate 9. A. leilia: A) LI (left side), AZ; B) LI (left side, head and thorax); C) LI
(front, head); D) LI (bottom, head and prothorax-note toothed mandibles
and neck gland; E) LI (bottom, proleg-note crampets); F) LI (rear, anal
segment).
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Plate 1 0. A. leilia: A) L2 (front, head), AZ; B) L2 (left side), AZ) C) L3 (front, head),
TX; D) diapause L3 (front, head-note stubby antlers), AZ; E and F)
diapause L3 (left side-note that abdominal segments 2-4 are duplicated
in this composite figure), AZ.
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Plate 11. A. leilia: A) L5 (front, head), TX; B) L5 (mandible-note undulating cutting
edge at lower left), AZ; C) L5 (front, left part of head capsule), AZ; D) L5
(side, right part); E) L5 (back, left part); F) P (left side and front, head),
TX.
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Plate 12. A. leillia: A) P (side, thoracic spiracular opening), TX; B) P (left side,
middle segments); C) P (left side, abdominal segments-note bent setae
and microfile on posterior edge of segment); D) P (left side, posterior
segments; E) P (left side and bottom, cremaster-note shortened bed of
hooks); F) P (bottom, cremastral hooks).
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Plate 13. A. clyton clyton: A) E (side-note scelionid emergence hole), VA; B) E
(micropyle); C) E (side near top); D) E (side nearer bottom).
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Plate 1 4. A. clyton texana: A) E cluster (top), AZ; B) E (micropyle); C) E (side near
top); D) E (side nearer bottom); E) LI (right side), TX; F) LI (right side,
head and prothorax).
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Plate 15.* A clyton louisa: A) L5 (front, right part of head capsule), TX; B) L5
(back, right part); C) L5 (side, left part).
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Plate 16. A. idyja argus: A) E (top-note scelionid emergence hole), Oaxaca,
Mexico; B) E (side, detail); C) L4 (front, head capsule), Oaxaca, Mexico;
D) L5 (front, left part of head capsule), Oaxaca, Mexico; E) L5 (back, left
part); F) L5 (side, right part).
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Plate 1 7. A. idyja argus: A) L5 (thoracic leg), Oaxaca, Mexico; B) L5 (thoracic leg,
detail of claw); C) L5 (mesal side, larval proleg-note crampets and
crochets), Oaxaca, Mexico; D) L5 (mesal side, larval proleg, detail).
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Plate 18.
A) A. celtis antonia eggs on C. laevigata, TX-note ripening rings.
B) A. leilia eggs on C. pallida, AZ.
C) A. clyton louisa eggs mass on C. laevigata, TX.
D) A. clyton clyton egg mass on C. occidentalis, VA-note scelionid
wasps.
E) A. celtis antonia diapause phase third instar larva, TX-lab reared.
F) A. celtis antonia fourth instar larva on C. reticulata, AZ.
G) A. leilia first instar larvae on C. pallida, AZ.
H) A. clyton clyton diapause phase third instar larvae, FL.
I) A. clyton clyton post-diapause third instar larva on C. laevigata, TX.
J) A clyton louisa second and third instar larvae on C. laevigata, TX.
K) A. celtis celtis fifth instar larva on C. occidentalis, VA.
L) A. celtis celtis fifth instar larva on C. laevigata, TX.
M) A. celtis antonia fifth instar larva on C. reticulata, TX.
N) A. celtis antonia fifth instar larva on C. laevigata, TX.
O) A. leilia fifth instar larva on C. pallida, AZ.
Plate 19. A) A. clyton clyton fifth instar larva on C. occidentalis, SE United
States.
B) A. clyton clyton fifth instar larva on C. tenuifolia Ml.
C) A. clyton texana fifth instar larva on C. laevigata, TX.
D) A. clyton texana fifth instar larva on C. reticulata, AZ.
E) A. clyton louisa fifth instar larva on C. laevigata, TX.
F) A. idyja argus fifth instar larvae on C. caudata, Oaxaca, Mexico.
G) A. celtis celtis pupa on C. laevigata, TX.
H) A. celtis antonia pupal case on C. reticulata, TX.
I) A. leilia pupa on C. pallida, AZ.
J) A. leilia pupa, TX.
K) A. clyton texana pupa, TX.
L) A. idyja argus pupa on C. caudata, Oaxaca, Mexico-diseased.
M) A. celtis antonia, female resting on C. reticulata, TX-dorsal basking.
N) A. celtis antonia, female resting on C. reticulata, TX-newly emerged.
O) A. clyton louisa, female resting on Ulmus sp., TX.
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J.Res.Lepid.
Plate 20. A. celtis celtis: A and B) male (dorsal and ventral), GA-reared; C) female
(dorsal), GA-reared.
A. celtis reinthali: D and E) male (dorsal and ventral), FL-holotype; F)
female (dorsal), FL-allotype.
A. celtis antonia: G and H) male (dorsal and ventral), N TX; I) female
(dorsal), N TX.
A. celtis antonia: J and K) male (dorsal and ventral), AZ-reared; L)
female (dorsal), AZ-reared.
A. celtis antonia: M and N) male (dorsal and ventral), S TX-reared; O)
female (dorsal), S TX-reared.
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J. Res. Lepid.
Plate 21. A leilia: A and B) male (dorsal and ventral), AZ-reared; C) female
(dorsal), AZ-reared.
A. clyton clyton: D and E) male (dorsal and ventral), PA-reared; F)
female (dorsal), PA-reared.
A. clyton clyton: G and H) male (dorsal and ventral), VA-reared; I) female
(dorsal), Ml-dark form, reared.
A. clyton flora: J and K) male (dorsal and ventral), FL-reared; L) female
(dorsal), FL.
A. clyton texana: M and N) male (dorsal and ventral), TX-reared; O)
female (dorsal), TX.
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J.Res.Lepid.
Plate 22. A clyton texana: A and B) male (dorsal and ventral), AZ-reared; C)
female (dorsal), AZ-reared.
A. clyton louisa: D and E) male (dorsal and ventral), Nuevo Leon,
Mexico; F) female (dorsal), TX-reared.
A. idyja idyja: G and H) male (dorsal and ventral), Cuba; I) female
(dorsal), Cuba.
A. idyja argus: J and K) male (dorsal and ventral), Sonora, Mexico-light
phase; L) female (dorsal), Veracruz, Mexico-light phase.
A. idyja argus: M and N) male (dorsal and ventral), Oaxaca, Mexico-dark
phase; O) female (dorsal), Veracruz, Mexico-dark phase.
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