LEPIDOPTERAN
BIODIVERSITY:
PATTERNS AND ESTIMATORS
M. Alma Solis
Michael G. Pogue
"Another advantage of the
attempt at mathematical
formulation is that it helps to
clarify which properties of the
components of a [biological]
system must be known if its
behaviour is to be predicted; in
other words, it tells us what we
nee d to measure. "
(J. Maynard Smith, Mathematical
Ideas in Biology, 1968)
206
T
HE
TERM
BIODIVERSITY
HAS MANY
DEFINI-
tions, one of which is the measurement
of species richness on a global basis
(Lovejoy 1997). Lepidopterans (moths and butterflies) are one of the most speciose groups of
organisms on Earth; the biological characteristics
instrumental in the success of this group are complex and interrelated. Examining patterns of diversity may be less than satisfactory because of the
varied ways of looking at species richness; as examples, richness can be examined taxonomically
(i.e., how many species of a certain group) or geographically (i.e., how many species in a particular
area). The fastest way to estimate species richness
of a taxon or of a geographic area is by compiling
data from the literature and/or using museum collections. However, to address specific conservation
issues, field collections and detailed taxonomic studies are vital to document and compare species richness among specific sites. Locality data on older
museum specimens sometimes is inadequate to
make conservation
decisions; therefore,
field
AMERICAN ENTO~1OLOGIST •
Winter 1999
collections become necessary to obtain useful data.
This especially is true of the larger groups in Lepidoptera
(e.g., Noctuoidea,
Geometroidea,
Pyraloidea, and Gelechioidea) because many areas
in the world that are suitable for studies of species
richness are poorly collected (e.g., the Pyraloidea
of Mexico; Solis 1996). Systematic studies determine the relationships
between species and provide information for identification.
Lepidopterans
are second to the coleopterans
in the Insecta in species richness. But lepidopterans
are the most popular because the order includes
butterflies (the birds of the insect world), which
always have attracted much attention. In fact, many
amateur and professional entomologists began as
butterfly collectors. Avocational interest in butterflies parallels that in birds so much so that butterfly watching is becoming nearly as popular as bird
watching.
In terms of species richness, there are many reasons why lepidopterans
have been relatively successful. Although caterpillars have an ubiquitous
source of food, feeding almost entirely on plants
or materials of plant origin, lepidopteran diversity
is in large part constrained or driven by competition for these very resources. The taxonomic range,
or specifically the chemical range, of food plants
and the variety of plant microhabitats,
such as
leaves, stems, roots, galls, seeds, and fruit, that can
be exploited for other purposes such as defense
against predation and parasitism (e.g., Bernays and
Chapman 1994) are a driving force in lepidopteran
evolution. Abiotic factors that could cause increase
in diversity include vicariance, climate change, or
are correct, the total may be as high as 280,0001,400,000 species for the world." Heppner (1991)
listed "total described" as 146,277 and "estimated
totals" as 255,000. Gaston (1991) listed estimates
from 112,000 to 165,000 given by four other entomologists and stated: "Discussion with several
lepidopterists suggests that an upper bound to the
overall size of the order of 500,000 species is reasonable, and that a figure somewhat lower is quite
probable." To illustrate more specifically where the
ambiguities about species numbers occur in the
phylogeny of the Lepidoptera, we arbitrarily chose
160,000 as the lower bound (Common 1990) and
500,000 (Gaston 1991) as the upper bound for
the total number of species.
The major ambiguities about species numbers
in the Lepidoptera occur in the moth groups. This
primarily nocturnal
portion of the order is the
larger in species numbers and has more impact on
the human condition because it includes many economically important pests of crops, ornamental
plants, and forests. It is estimated that there are
17,500 butterfly species in the world and that 90%
of them have been described (Robbins and Opler
1997). Subtraction of the number of butterfly species, 17,500, from the total Lepidoptera lower and
upper bounds of species numbers implies that there
may be between 142,500 and 482,500 species of
moths.
plate
tion
tectonics.
River
dynamics
in western
Amazonia that cause high site turnover, disturbance
and variation in forest structure, and primary succession on riverine soils caused by meandering rivers, may be major factors creating and maintaining
between habitat species diversity (Salo et al. 1986).
Less common than herbivores in the Lepidoptera
are predators, parasites, or even detritivores, whose
life-styles have evolved independently in several lepidopteran families. As a selective pressure predation upon lepidopterans has played a major role in
the evolution and diversification of groups within
the order, particularly with respect to bat predation (e.g., Fullard and Yack 1993, Rydell et al.
1995). Tympanal organs, or "ears," have evolved
independently at least three times in Lepidoptera.
In three of the most successful groups of moths
(i.e., groups with more than ten thousand species),
most species can detect bat ultrasound and evade
predation. Butterflies and a minority of moths that
are diurnal, and small moths that do not fly in
open areas, are not likely to be subject to bat predation. Instead, they have evolved strategies such
as aposematism
and camouflage to evade avian
and other diurnal predators.
Many entomologists
have estimated the total
number of species of Lepidoptera. In 1976, Hodges
stated: "The described, world fauna of Lepidoptera
is more than 140,000 species, and if projections
AMERICAN ENTOMOLOGIST'
Volume 45, Number 4
Phylogenetic Patterns of Species
Richness
To illustrate
of species
lepidopteran
number
diversity, a combina-
estimates
from Heppner
(1991) and Scobie (1992) for families and superfamilies are superimposed on modern phylogenies
of the Lepidoptera (Minet 1991, Scobie 1992) (Figs.
1-3). The Lower Lepidoptera (Fig. 1) are comprised
of approximately
2,035 described species (Scobie
1992). Within the Lower Lepidoptera, phylogenetic relationships are fairly well resolved-superfamilies are small, and species estimates are accurate.
The next, more advanced group is the Ditrysia
(Figs. 2 and 3) (Minet 1991). These are lepidopterans with two separate apertures in the female genitalia (one for mating, one for egg laying). Subtraction of the number of Lower Lepidoptera species,
2,035, from the total lepidopteran lower and upper species estimates (Common
1990, Gaston
1991) leaves between 140,465 and 480,465 species of moths for the entire Ditrysia.
The phylogeny is less well resolved in the Lower
Ditrysia (Fig. 2) than in the Lower Lepidoptera,
and there has been an increase in size from families
with tens and hundreds of species to families with
thousands of species. Based on estimates from the
literature (Heppner 1991; note, some figures are
overestimated in the Ditrysia; see also Scobie et al.
1995) there are approximately 34,600 species in
the Lower Ditrysia. However, this number is highly
misleading. For example, the Gelechioidea contain
207
These are large superfamilies where the monophyly
is clear; however, at lower taxonomic levels, monophyly is unsupported
or groups clearly are polyphyletic. There has been an increase in species richness from groups in the Lower Ditrysia with thousands of species to groups in the Higher Ditrysia
with tens of thousands of species (Heppner 1991).
Subtraction of the number of Lower Ditrysian species, 34,600, from the 140,465 and 480,465 lower
and upper total species estimates leaves a broad
range of approximately
105,865 and 445,865 estimated species for the Higher Ditrysia (not including the butterflies). The lack of phylogenetic information is strongly correlated with an uncertainty
about species numbers. The circular ramification
of these results is clear-in
large groups such as the
Higher Ditrysia, there are not enough taxonomic
researchers and, therefore, species identities and
relationships are still unknown and numbers only
5
8
7 1
5 7
4 9
10
1 8
Lower Lepidoptera=2,035
spp.
Fig. 1. Numbers of species for each family in phylogeny of Lower
Lepidoptera (from Scobie 1992, but also see Kristensen 1984);
phylogeny of Ditrysia continued on Figs. 2 and 3.
5,8 0
16, 00
6, 00
Apodit ysia
Cit sia
Fig. 2. Numbers of species for selected superfamily groups in
phylogeny of Lower Ditrysia (from Minet 1991); phylogeny of
Obtectomera or Higher Ditrysia continued on Fig. 3.
species, and R. W. Hodges (personal communication), a gelechioidean specialist, estimates that there
are, additionally, at least as many undescribed as
decribed species (i.e., approximately
16,600). This
may be true of many of the larger superfamilies in
the Lower Ditrysia.
Phylogenetic relationships in the Higher Ditrysia
(Fig. 3), or Obtectomera,
are highly unresolved.
These are lepidopterans with pupae that have no
mobility in the first three abdominal
segments.
208
can be estimated.
Some systematists
are compiling preliminary
estimates of species richness in lepidopteran groups
using museum collections and the literature. Although, providing general numbers for large geographic areas, there are inherent problems that
make these studies extremely preliminary. For example, butterflies are the best known group in the
order. As part of the Biological Diversity of Guyana
project at the Smithsonian Institution, data were
compiled for seven genera of butterflies from major museums in the United States and several museums in England. For most specimens, label data
were general with "Guyana" as the only information. Specimens labeled with more precise collecting localities showed a conspicuous bias toward
areas that are most easily accessible or popular
vacation destinations (unpublished data). The resulting data were nearly useless for within-country
decisions about conservation and land use.
Estimating species richness for the order based
on the existing literature can be biased by the moth
body size as shown from taxonomic
studies of
pyraloid moths collected as part of an inventory in
Costa Rica. For example, members of the genus
Omiodes (Crambidae: Spilomelinae) are 4 times
larger in wing length than members
of the
Glaphyriinae (Crambidae) (Solis 1997, Gentili and
Solis 1998, Solis and Adamski 1998). Most of these
larger moths had been described more than once
(i.e., have numerous synonyms; see also ScobIe et
al. 1995), the smaller moths had not been collected
adequately, and a higher percentage (27%) were
undescribed (Solis 1997).
Site-specific Patterns of Species
Richness and Complementarity
Museum collections and existing literature may
provide the data for preliminary estimates of species richness, but reliable numbers come only from
well-designed biodiversity projects that effectively
utilize field collecting of target taxa and analyses by
mathematical models that calculate site-specific spe-
AMERICAN
ENTOMOLOGIST
•
Winter 1999
cies richness. These methods represent a more meaningful starting point for addressing the question of
world insect diversity. Inventories or species lists
from different sites can be compared to measure
relative levels of overlap (complementarity
or biotic distinctness)
and richness of specific taxa
around the globe. After a site has been sampled,
species richness estimators can be used to predict
the number of species that were missed during the
sampling process, thus arriving at an estimate of
species based on the actual number observed plus
the predicted number missed. By using species lists,
generated either by field sampling or from museum
collections, species composition between sites can
be compared. These studies can be conducted in
any geographic area (e.g., even in a backyard with
any group of animals or plants).
In the rest of this article, we present three examples of such studies in Lepidoptera: (1) a preliminary survey of the Lepidoptera (excluding butterflies) measuring complementarity
between two
rainforest sites; (2) the use of the notodontid moth
genus Hemiceras, with 245 species (Pogue, unpublished), to estimate
species richness at three
rainforest sites; and (3) the use of Hemiceras to
compare species composition among sites in South
America using dissimilarity matrices and cluster
analysis. We now will describe how rigorous sampling methods combined with mathematical models using unpublished data can provide compelling
estimators of species richness.
Ty
16, 00
The lepidopteran faunas of Pakitza, Peru, and
Beni, Bolivia, were compared
using complementarity, a measure of the distinctness or dissimilarity of a specific site in comparison with one or
more other sites (i.e., the higher the value, the fewer
taxa the sites have in common
(Colwell and
Coddington 1994). Thirty-eight families were collected from both sites, but only nine families had
numbers of species sufficient to illustrate trends in
complementarity.
Five of these families were "microlepidoptera"
(primitive, small moths; not a
monophyletic group [Figs. 2 and 3]); Pyralidae and
Crambidae were considered as one group because
they are sister
groups
in the Pyraloidea;
Cosmopterigidae and Gelechiidae are Gelechioidea;
Tineidae are Tineoidea). The remaining four were
"macrolepidoptera"
(derived large moths; the
monophyletic
group Macrolepidoptera
(Fig. 3);
Geometridae
are Geometroidea;
Noctuidae,
Notodontidae,
and Arctiidae are Noctuoidea).
In
these nine families, 1,731 specimens representing
1,006 species were collected at Pakitza in 12 trap
nights and 1,748 specimens representing 933 species at Beni in 8 trap nights. The "microlepidopteran" families had higher complementarity
(or
distinctness)
values (100-96.8 %), than the
"macrolepidopteran"
families (95.2-91.5%), with
the exception of the Noctuidae (98.6%) (Tables 1
AMERICAN ENTOMOLOGIST.
Voillme 45, Nllmber 4
42, 00
Macrolep doptera
Obtec omera
(or High r Ditrysia)
Fig. 3. Numbers of species for selected superfamily groups in
phylogeny of Higher Ditrysia (from Minet 1991).
Table 1. Comparison of % complementarity and number of species of "microlepidoptera"
between Pakitza, Peru, and Beni, Bolivia
Family
The Lepidoptera and Complementarity
Between Two Sites
ana
org ns
% Complementarity
No. of Species (shared)
Cosmopterigidae
100.0
50
(0)
Tineidae
100.0
113
(0)
Gelechiidae
98.8
167
(2)
Oecophoridae
97.8
324
(7)
Pyralidae/Crambidae
96.8
281
(9)
Table 2. Comparison of % complementarity and number of species of
"macrolepidoptera" between Pakitza, Peru, and Beni, Bolivia
Family
% Complementarity
No. of Species (shared)
Noctuidae
98.6
296
(4)
Notodontidae
95.2
63
(3)
Geometridae
93.3
213
(14)
Arctiidae
91.5
189
(16)
and 2). The lower complementarity
found in most
"macrolepidoptera"
compared to the "microlepidoptera" may have been due to sampling bias because collecting was by an ultraviolet light, and
larger moths may have been coming from a larger
"collecting universe" than smaller moths. Alterna-
209
40
species are known for their migratory behavior
and dispersal abilities. The answer may be their
diversity. Noctuidae is the most species-rich lepidopteran family, and the sampling time may have
been inadequate to assess accurately the ranges of
many noctuid species resulting in an inflated
complementarity value. Seasonality, weather, or
unknown yearly population fluctuations are other
factors that could influence species richness; therefore, sampling year round would result in a more
nearly accurate estimate of noctuid, and more
broadly lepidopteran, complementarity.
35
30
.•••
25
'u
••
Co
Ul
20
'0
o
z
Hemiceras and Species Richness at
Three Sites
15
.-+- Pakitza
,-+-
10
-..-
Tambopata
Onkone Gare
5 -
02
345
6
7
8
9
10
11
12 13 14
15 16
17 18 19 20 21 22 23
Collecting Days
Fig. 4. Species accumulation curves of Hemiceras
Tambopata, Peru, and Onkone Gare, Ecuador.
at Pakitza and
Fig. 5. Six western Amazonian sites used in cluster analyses of
dissimilarity matrices; (1) Neblina, (2) Onkone Gare, (3) Sao Paulo de
Oliven~a, (4) Porto Velho, (5) Pakitza, (6) Tambopata.
tively, the "macrolepidopteran" faunas truly may
be less distinct because larger moths may have
greater dispersal abilities than smaller moths. The
relaliYdr
hif \QlUf'\rn\n\~mr il~i\m\l~i~~
m ~[[[ [lilt l~ij~
~[tim l~li~~~[ij\!,
l!mM, II
the Noctuidae is curious given that they are generally strong fliers, medium to large moths, and many
210
A preliminary inventory to estimate species richness of Hemiceras was conducted at three rainforest
sites: Pakitza (Rio Manu) and Tambopata Reserved
Zone (Rio Tambopata) in southeastern Peru, and
Onkone Gare Camp (near Yasuni National Park)
in Ecuador. To estimate accurately the total number of species at a particular site, the species accumulation curve (or the associated curve of a suitable richness estimator) should reach an asymptote and remain constant over time or with additional sampling (Fig. 4). Of the three sites, the species accumulation curve reached an asymptote only
at Pakitza suggesting that the species estimate for
this locality was the most nearly accurate. Although
it may appear that the species accumulation curve
reached an asymptote at Onkone Gare, the number of collecting days should have been equal to
that of Pakitza for a valid comparison. Tambopata
is known for high species richness of various insect
groups (Fisher 1985, Paulson 1985, Pearson 1985,
Wilkerson and Fairchild 1985, Robbins et al.
1996). In contrast, the Hemiceras fauna was poor
at Tambopata with only 24 species, considering
that there were 245 species in the Neotropical Region (Pogue, unpublished
data). Although
Hemiceras samples taken at Tambopata and
Onkone Gare were insufficient to estimate accurately species richness, as shown by nonasymptotic
species accumulation curves, it appears that after
seven trap days, Pakitza was more species rich than
Tambopata based on all nonparametric estimates
(Pogue, unpublished data) and the steeper accumulation curve. This contrasts with a study of the
faunal relationships between the Cicadoidea
(Homoptera) (Pogue 1996) and Odonata (Louton
et al. 1996) at Pakitza and Tambopata where the
resulting species richness was greater at Tambopata.
Thus, either the preliminary estimate for Hemiceras
at Tambopata was inaccurate, or this study demonstrated that different taxa, with divergent biologies, have different centers of diversity. Based on
the species richness data for Hemiceras, the following criteria are recommended for follow-up studies. First, the species accumulation curve or esti-
there is a preponderance of rare species (singletons), Chao 1 should give the higher and, perhaps,
AMERICAN
ENTOMOLOGIST
•
Winter 1999
best estimate [Chao 1 is an estimator of the true
number of a species at a given site based on the
number of rare species in one pooled sample]; and
if the number of rare species is low, Chao 2 (or the
second-order jackknife) should give a better estimate [Chao 2 is an estimator based on the incidence of rare species among numerous samples]
(see Corwell and Coddington 1994 for further discussion). It also is important for rapid assessment
to choose the target taxon in a particular area carefully. The target taxon has to be common throughout the study area so that it can be sampled easily,
and rare species must not be dominant. If rare species are dominant, the study could require years to
reach an asymptote. Alternatively, a taxon with
too many species (more than 400 species) would
not allow rapid assessment because more samples
would have to be taken, and it would take longer
to process specimens and retrieve data. In the
Neotropics, a target taxon of 200-400 species, such
as cicadas (Pogue 1996) and Hemiceras (Pogue,
unpublished data), seems to be large enough for
species accumulation curves to reach an asymptote
after 20-30 samples, in this case trap-days.
Hemiceras and Complementarity
Among Six Sites
Species lists of Hemiceras were compiled from
specimens in the National Museum of Natural History, Smithsonian Institution, Washington, D.C.,
and used to examine faunal relationships among
sites in South America. Six sites were chosen to
determine
fa unal relationships
in western
Amazonia: Pico de Neblina (1), Venezuela; Onkone
Gare Camp (2), Ecuador; Sao Paulo de Olivent;a
(3) and Porto Velho (4), Brazil; and Pakitza (5) and
Tambopata
(6), Peru (Fig. 5). Complementarity
values between sites were used to produce dissimilarity matrices, which were converted into dendrograms using cluster analysis (SYSTAT 1992). The
complementarity
values of the nodes on the dendrogram show that Pakitza (Peru) and Tambopata
(Peru) were the least dissimilar, or had more taxa
in common than with other sites (Fig. 6). Porto
Velho (Brazil) had the highest complementarity
value and, therefore, the fewest number of species
in common with all other sites. As expected,
complementarity
seemed affected strongly by habitat and distance. If the habitat is similar, the fauna
is less dissimilar and the complementarity
is less; if
distance increases between two sites, there is an
increase
in
dissimilar
fauna
and
the
complementarity
is greater. Pakitza and Tambopata
(Peru), similar in habitat and only 500 km apart,
had the least dissimilar fauna; Onkone Gare (Ecuador) and Neblina (Venezuela), similar in habitat,
but approximately
1,160 km apart, had the next
least dissimilar fauna (Fig. 6). On a broader biogeographic scale, Amazonia often is treated as one
large area, but these results show that faunistic
relationships
among species of Hemiceras at the
western Amazonia
sites (Pakitza, Tambopata,
AMERICAN ENTOMOLOGIST
•
Volume 45, Number 4
Porto Velho (4)
Sao Paulo de Olivenca (3)
Pakitza (5)
Tambopala (6)
Neblina (1)
Onkone Gare (2)
0.806 0.833
I
I II
I
0.766 0.7930.815
Fig. 6. Dendogram for cluster analysis of dissimilarity matrix of
western Amazonian sites. Numbers refer to sites in Fig. S. The scale
indicates complementarity values.
Onkone Gare and Neblina) are distinct from the
eastern Amazonia sites (Porto Velho and Sao Paulo
de Oliven<;a [Brazil]) (Fig. 6).
Conclusions
Lepidopterans are the most popular and one of
the most diverse groups in the Insecta. Species richness and diversity can be attributed most reliably
to the exploitation of a great diversity of architectural and chemical features of vascular plants by
the immature stages. Success of the most speciose
groups in the Lepidoptera can be attributed partially to the development of unique morphological
structures,
novel behavioral
patterns, complex
chemical strategies that protect them against predation and/or parasitism, or abiotic selection factors such as vicariance or climatic change. Species
richness in the derived moth taxa with over tens of
thousands of species only can be estimated because
there is a lack of taxonomic information. Estimates
of species richness based on taxonomic names in
the literature can be misleading due to unrecognized synonyms and because small moths are less
well collected than large moths. Museum collections can be useful for generating preliminary information, but, ultimately, field studies are necessary to assess diversity. When data from similar
studies are pooled, complementarity
or distinctness between sites can be calculated and used to
predict species numbers at other sites. Examples of
studies from South America demonstrate that sitespecific data analysis is a prerequisite to a thorough understanding
of regional diversity patterns.
Species lists, species richness estimates,
and
complementarity
values generated from taxonomic
studies and biodiversity inventories can be used by
biologists and laypersons to make more informed
decisions about land use and conservation.
Acknowledgments
We gratefully recognize these institutions and
programs designed to inventory and study the biological diversity of organisms and that supported
our research: Instituto Nacional de Biodiversidad
(INBio), Costa Rica, and Office of Biodiversity Pro-
211
grams, National
Museum of Natural
History,
Smithsonian
Institution,
Washington,
D.C. We
thank T. L. Erwin, Smithsonian Institution, Washington, D.C.; E. E. Grissell, J. W. Brown, and D. R.
Smith, Systematic Entomology Laboratory, USDA,
Washington, D.C.; R. L. Brown, Mississippi State
University, Mississippi State, MS; and R. W. Hodges,
Eugene, OR, for comments on the manuscript.
References
Cited
Bernays, E. A., and R. F. Chapman. 1994. Host-plant
selection by phytophagous insects. Chapman & Hall,
New York.
Colwell, R. K., and J. A. Coddington. 1994. Estimating
terrestrial biodiversity through extrapolation. Phil.
Trans. Roy. Soc. London. 345: 101-118.
Common, LF.B. 1990. Moths of Australia. Melbourne
University Press, Carlton, Victoria.
Fisher, E. M. 1985. A preliminary list of the robber flies
(Diprera: Asilidae) of the Tambopata Reserved
Zone, Madre de Dios, Peru. Rev. Peruana Entomol.
27: 25-36.
Fullard, J. H., and J. E. Yacko 1993. The evolutionary
biology of insect hearing. Tr. Ecol. Evol. 8: 248252.
Gaston, K. J. 1991. The magnitude of global insect
species richness. Conserv. BioI. 5: 283-296.
Gentili, P., and M. A. Solis. 1998. Checklist and key of
New World species of Omiodes Guenee with descriptions of four new Costa Rican species (Lepidoptera: Crambidae). Entomol. Scand. 28: 471492.
Heppner, J. B. 1991. Faunal regions and the diversity of
Lepidoptera. Trop. Lepidop. 2 (Suppl. 1): 1-85.
Hodges, R. W. 1976. Presidential address 1976-What
insects can we identify? J. Lepidop. Soc. 30: 245251.
Kristensen, N. P. 1984. Studies on the morphology and
systematics of primitive Lepidoptera (Insecta).
Steenstrupia 10:141-191.
Louton, J. A., R. W. Garrison, and O. S. Flint. 1996.
The Odonata of Parque Nacional Manu, Madre de
Dios, Peru; natural history, species richness and comparisons with other Peruvian sites, pp. 431-449. In
D. E. Wilson and A. Sandoval
[eds.], La
Biodiversidad
del Sureste del Peru: Manu
Biodiversity of Southeastern
Peru). Editorial
Horizonte, Lima, Peru.
Lovejoy, T. E. 1997. Biodiversity: What Is It?, pp. 714. In M. Reaka-Kudla, D. E. Wilson, and E. O.
Wilson [eds.], Biodiversity II: Understanding and
protecting our biological resources. Joseph Henry
Press, Washington, D.C.
Minet, J. 1991. Tentative reconstruction of the ditrysian
phylogeny (Lepidoptera:
Glossata). Entomo!.
Scand. 22: 69-95.
Paulson, D. R. 1985. Odonata of the Tambopata Reserved Zone, Madre de Dios, Peru. Rev. Peruana
Entomol. 27: 9-14.
Pearson, D. L. 1985. The tiger beetles (Coleoptera:
Cicindelidae) of the Tambopata Reserved Zone,
Madre de Dios, Peru. Rev. Peruana Entomol. 27:
15-24.
Pogue, M. G. 1996. Biodiversity of Cicadoidea
(Homoptera) of Pakitza, Manu Reserved Zone and
Tambopata Reserved Zone, Peru: A faunal com-
212
parison, pp. 313-325. In D. E. Wilson and A.
Sandoval [eds.], La biodiversidad del sureste del
Peru: Manu (Biodiversity of Southeastern Peru).
Editorial Horizonre, Lima, Peru.
Robbins, R. K., G. Lamas, O. H. Mielke, D. J. Harvey,
and M. M. Casagrande. 1996. Taxonomic composition and ecological structure of the species-rich
butterfly community at Pakitza, Parque Nacional
del Manu, Peru, pp. 217-252. In D. E. Wilson and
A. Sandoval [eds.], La Biodiversidad del Sureste del
Peru: Manu (Biodiversity of Southeastern Peru).
Editorial Horizonte, Lima, Peru.
Robbins, R. K., and P. A. Opler. 1997. Butterfly diversity and a preliminary comparison with bird and
mammal diversity, pp. 69-82. In M. Reaka-Kudla,
D. E. Wilson, and E. O. Wilson [eds.], Biodiversity
II: Understanding and protecting our biological resources. Joseph Henry Press, Washington, D.C.
Rydell, J., G. Jones, and D. Waters. 1995. Echolocating
bats and hearing moths: who are the winners? Oikos
73: 419-1995.
Salo, J., R. Kalliola, I. Hakkinen, Y. Makinen, P.
Niemela, M. Puhakka, and P. D. Coley. 1986. River
dynamics and the diversity of Amazon lowland forest. Nature 322: 254-258.
Scobie, M. J. 1992. The Lepidoptera: form, function
and diversity. Oxford University Press, Oxford, England.
Scobie, M. J., K. J. Gaston, and A. Crook. 1995. Using
taxonomic data to estimate species richness in
Geometridae. J. Lepidop. Soc. 49: 136-147.
Solis, M. A. 1996. Pyraloidea (Lepidoptera), pp. 521531. In J. Llorente, Alfonso N. Garcia, and Enrique
Gonzalez [eds.], Biodiversidad,
taxonomia
y
biogeografia de artropodos de Mexico: Hacia una
sintesis de su conocimiento, Universidad Nacional
Autonoma de Mexico, Mexico.
Solis, M. A. 1997. Snout moths: unraveling the taxonomic diversity of a speciose group in the Neotropics,
pp. 231-242. In M. Reaka-Kudla, D. E. Wilson,
and E. O. Wilson [eds.], Biodiversity II: Understanding and protecting our biological resources. Joseph
Henry Press, Washington, D.C.
Solis, M. A., and D. Adamski. 1998. A review of Costa
Rican Glaphyriinae
(Lepidoptera:
Pyraloidea:
Crambidae). J. N. Y. Entomol. Soc. 106: 1-55.
SYSTAT. 1992. Statistics, version 5.2 edition. SYSTAT
Inc., Evanston, IL.
Wilkerson, R. C., and G. B. Fairchild. 1985. A checklist
and generic key to the Tabanidae (Diptera) of Peru
with special reference to the Tambopata Reserved
Zone, Madre de Dios, Peru. Rev. Peruana Entomol.
27: 37-53.
•
M. Alma Solis is a Research Entomologist working on the systematics of the Pyraloidea with the
Systematic Entomology Laboratory, USDA. She
is currently on loan to The University of Texas at
Brownsville/Texas South most College where she
is an Associate Dean of the College of Science,
Math & Technology, and Interim Chair of the Department of Biological Sciences. Michael G. Pogue
is a Research Entomologist in the Systematic Entomology Laboratory, USDA, Washington, D.C.
His research interests are in the systematics,
biodiversity, and higher level classification of the
Noctuidae.
AMERICAN
ENTOMOLOGIST
•
Winter 1999