SYSTEMATICS
A New Cryptic Species of Cicada Resembling Tibicen dorsatus
Revealed by Calling Song (Hemiptera: Auchenorrhyncha: Cicadidae)
JEFFREY A. COLE1
EEB Department, University of Kansas, 1200 Sunnyside Avenue, Lawrence, KS 66045
Ann. Entomol. Soc. Am. 101(5): 815Ð823 (2008)
ABSTRACT Two morphologically cryptic species have until now been treated under the name
Tibicen dorsatus (Say). T. dorsatus is redescribed, and a neotype is designated from topotypic material
collected from Atchison County, KS. Tibicen tremulus sp. n. is described and diagnosed from T. dorsatus
and from similar species by using the shape of the male claspers and color pattern. Calling songs of
the males are distinct, as evidenced by Þeld recordings of multiple individuals of both species. Males
of T. dorsatus produce a rattling song, during which syllables are repeated at a rate of 38.9 ⫾ 1.7 s⫺1
and are broadcast over a constant carrier frequency band of 2.6 Ð12.7 kHz, 4.0 ⫾ 0.3 kHz at maximum
amplitude. The main portion of the song of T. tremulus consists of amplitude and frequency modulated
syllables repeated at a rate of 16.2 ⫾ 0.6 s⫺1, frequency 5.4 ⫾ 0.3 kHz at maximum amplitude. During
these modulations, amplitude increases and a base frequency range of 3.9 Ð5.8 kHz broadens to 3.6 Ð7.7
kHz for a duration of 19.7 ⫾ 2.7 ms. Dorsoventral movements of the male abdomen accompany the
amplitude and frequency modulations in T. tremulus, a behavior not observed in singing males of T.
dorsatus. Museum records show T. dorsatus to be widespread in the prairie biome of the central United
States. T. tremulus occurs west of ⫺97⬚ longitude, where it seems to be widely if not entirely sympatric
with T. dorsatus.
KEY WORDS Cicadidae, Tibicen, cryptic species, bioacoustics
Large numbers of morphologically cryptic species are
likely to exist in nature (Bickford et al. 2006), and
analyses of behavioral premating isolation mechanisms are powerful means of discovering them. The
songs of acoustic insects are one such behavioral isolation mechanism (Wells and Henry 1998), and studies of insect songs have revealed the presence of large
numbers of cryptic species within such familiar groups
as the crickets and katydids (Orthoptera: Gryllidae,
Tettigoniidae) (Alexander 1957, Walker et al. 2003),
and the cicadas (Hemiptera: Cicadidae) (Sueur and
Puissant 2007). Once species boundaries have been
delimited through behavioral analyses, morphological
characters that were subtle or previously overlooked
may then be discovered, enabling the identiÞcation of
preserved specimens (Walker et al. 1973).
Closely related species of cicadas tend to be morphologically similar. A recent song-based study revealed a cryptic species within the extensively studied
North American periodical cicada genus Magicicada
(Marshall and Cooley 2000), underscoring the power
of acoustic analysis in delimiting species boundaries
within the Cicadidae. The majority of United States
cicada diversity occurs in the western states (Davis
1944). Most western species remain poorly known,
and new species continue to be described from this
1
Corresponding author, e-mail: [email protected].
region (e.g., Heath and Sanborn 2007). This study adds
a species to the genus Tibicen, the North American
members of which are comparatively well known. The
last taxon of Tibicen described from the United States
was T. bifidus simplex Davis, 1941 from Arizona, distinguished by male genitalic morphology.
Say (1825) described Cicada dorsata from the
Konza Village, what is today the vicinity of Atchison
in northeastern Kansas (Kondratieff et al. 2002). This
name, transferred to the genus Tibicen by Van Duzee
(1916), is currently applied to the large testaceous and
black cicadas with a prominent middorsal row of pruinose spots on the abdominal tergites (Lawson 1920,
Froeschner 1952, Kondratieff et al. 2002). Cicadas
possessing this habitus are common inhabitants of
herbaceous vegetation throughout the prairies of the
central United States. During Þeldwork in Kansas and
eastern Colorado from 2005 to 2007, I noted that cicadas resembling T. dorsatus produce two qualitatively
different calling songs: a rattling song heard commonly
in the eastern portion of the range, and a trembling
song heard only in the west. At Picture Canyon, Baca
Co., CO, I heard both song types produced syntopically. Observations of calling males at this locality
conÞrmed that each individual male produces only
one of the two song types, that males producing a
particular song type tend to chorus with other males
of their song type and that distinct behaviors accom-
0013-8746/08/0815Ð0823$04.00/0 䉷 2008 Entomological Society of America
816
ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA
pany the production of each song type. Recordings of
males provided quantitative evidence that the songs are
distinct. Examination of preserved males of known song
type and associated females revealed consistent differences in the color pattern and the male genitalia. I concluded that two species are involved, reproductively
isolated in sympatry through differences in calling song.
SayÕs type material of Cicada dorsata is apparently
lost (Kondratieff et al. 2002), so I designate a neotype
from Atchison County, KS, and redescribe Tibicen
dorsatus (Say). I describe Tibicen tremulus, sp. n., and
highlight morphological features that allow the majority of preserved specimens to be identiÞed. Based
on recordings of topotype males, I show that the rattling song type belongs to T. dorsatus and the trembling song type belongs to T. tremulus, sp. n. I present
an analysis of the calling songs quantitatively demonstrating their distinctness, and discuss species-speciÞc
behavioral differences in the production of the two
songs. I estimate the ranges of the two species based
on museum specimen records.
Materials and Methods
Specimens. The species descriptions in this paper
are based primarily on the type specimens, but they
include notes on variability obtained from examining
series. Morphological terminology follows that of
Moulds (2005). I examined specimens from the Snow
Entomological Museum, University of Kansas (SEMK);
the Enns Entomological Museum, University of Missouri
(EMUM), the C. P. Gillette Museum of Arthropod
Biodiversity, Colorado State University (GMCS); the
K. C. Emerson Entomology Museum, Oklahoma State
University (EMOS); the Texas A&M University Insect
Collection (TAMU), and the Museum of Entomology
and Prairie Arthropod Research, Kansas State University
(MEKS). I used Vernier calipers to measure specimens,
which are given in the format range, mean ⫾ SD (millimeters). Head measurements include the eyes, and
pronotum measurements were made across the suprahumeral plates. I deposited all type material at SEMK.
Calling Song Recording and Analysis. I recorded
calling songs in the Þeld using a shotgun microphone
(model C451E, AKG, Vienna, Austria) and DAT recorder (model DA-P1, TEAC America, Montebello,
CA), capturing frequencies up to 18 kHz. This equipment recorded all major sound energy, which lies
below the ultrasonic threshold of 20 kHz. I used a
shotgun microphone because the cicadas startled
readily and exhibited “sing-ßy” behavior, making them
difÞcult to approach. Most were recorded at a distance
of 1 m or greater. Males of the different species were
in some instances positioned close to one another, so
care was taken when matching recordings with specimens. I did not measure ambient temperatures because cicadas thermoregulate, making ambient temperature an unreliable measure of the physiological
temperature of a singing male (Sanborn 1997).
I digitized recordings with BatSound Pro (Pettersson Elektronik AB 2001) at a sampling rate of 44.1 kHz.
I Þltered all recordings below 1 kHz to remove wind
Vol. 101, no. 5
and other ambient noise, by using a Butterworth highpass Þlter in BatSound. Data on syllable length and
peak frequency were extracted using the pulse characteristics feature of BatSound and veriÞed by eye.
Frequency ranges were measured from spectrograms
generated in BatSound with a fast Fourier transformation algorithm. Individual sound pulses were not
clearly deÞned on the oscillograms and thus were not
counted. I performed statistical analyses in Minitab,
version 13 (Minitab Inc. 2000). Temporal parameters
and peak frequencies are reported as means. Medians
are reported for the lower and upper bounds of frequency ranges. Oscillograms and spectrograms shown
in Figs. 3 and 4 were generated with Raven Lite,
version 1.0 (Cornell Lab of Ornithology 2007).
Distribution. I estimated the ranges of both species
by examining 332 specimens of T. dorsatus (215 males
and 117 females) and 125 specimens of T. tremulus (92
males, 33 females). Coordinates of localities visited
personally were obtained with a GPS receiver. For
museum specimens bearing labels with speciÞc localities, I used an online place names index (placenames.com) to obtain approximate coordinates. County
records without speciÞc localities were plotted in the
midpoint of the counties. Whenever possible, speciÞc
localities within counties were plotted in lieu of the
midpoints. I generated the distribution map with
ArcGIS, version 9.2 (ESRI 2006).
Results and Discussion
Tibicen dorsatus (Say, 1825)
(Figs. 1A [male genitalia], 2A [habitus], 3AÐC [song],
5 [distribution]).
Cicada dorsata Say 1825: 331. Type locality: Konza
Village, MO Territory. Type material lost.
Thopha varia Walker 1850: 42.
Fidicina crassa Walker 1858: 10.
Tibicen dorsata Van Duzee 1916: 55. [Catalogued;
transferred to Tibicen Latreille].
Tibicen dorsatus Metcalf 1963: 261. [Catalogued; speciÞc epithet changed to agree with gender of genus].
Description. NEOTYPE: 1 male, USA, KS, Atchison
Co., Atchison State Fishing Lake, 7 miles. NW of
Atchison, 39.6315⬚ N, 95.1742⬚ W, 285 m. 26-VIII-2007,
specimen no. AT07-01, J. A. Cole, W. ChatÞeld-Taylor.
TOPOTYPES: 5 males, 2 females, same data as neotype.
Head. As wide to slightly wider than anterior margin of pronotum, covered with Þne gold hairs. Rostrum
brown with black tip, extending caudally to metathoracic basisternum. Anteclypeus brown medially, black
laterally. Postclypeus brown anteriorly, black dorsally,
transverse grooves black, Þlled with sparse golden
hairs. Lora black, fading to brown anteriorly, with
brown margins. Genae tan. Supra-antennal plates
brown ventrally with a black stripe along anterior
margin from eye to postclypeus, dorsally brown, enclosing small black spots anteriorly, one on each side
September 2008
COLE: A NEW CRYPTIC SPECIES OF Tibicen
817
Fig. 1. Male terminalia, ventral view. (A) T. dorsatus. (B) T. tremulus sp. n.
of postclypeus. Antennae brown with black annuli or
with dorsal surface darkened. Frons with brown triangle, its base situated at postclypeus, pointing caudally toward median ocellus. Vertex black, a small
brown mark laterad of each lateral ocellus, brown
crescents covering posterolateral two thirds.
Thorax. Pronotal collar brown with anterior portion black, lateral margins trimmed with black. Within
collar, black with following areas brown: a middorsal
stripe, two small anteromedial diagonal ovate spots
mesal to paramedian Þssures, two large lateral spots
occupying lateral two thirds of pronotum. Mesonotum
background black. A pair of tan J-shaped marks originate at or posterior to the pronotal collar on the
middorsal line, extend posteriorly onto scutum, bend
laterally and anteriorly around posterior border of
parapsidial suture and then widen caudally to contact
anterior arms of cruciform elevation. A small pruinose
spot generally covers anteromedial emanation of the
J-marks, but it is faint or absent in some specimens.
Lateral sigilla with two narrow to wide red-brown
oblique stripes extending anterolaterally from wide
ends of J-marks to anterolateral corners of scutum. A
pair of pruinose spots extends posterolaterally along
the parapsidial sutures from collar to wide end of
J-marks. Lateral margins of mesonotum with heavy
pruinose bands. Scutellum brown, anterior arms of
cruciform elevation black apically, enclosing two pruinose spots anteriorly which join to form a large pruinose diamond in some specimens. Posterior arms of
cruciform elevation enclose pruinose spots laterally.
Wing grooves dark brown, faintly pruinose. Prosternum tan, meso- and metasterna black, pruinose. Pleura
black with tan sutures, pruinose.
Legs. Brown, coxae darker laterally, with small
black spot near apex. Ridge on forefemoral ßexor
surfaces black, spines brown. Metatibiae with black
tibial combs, variable number of black spurs on apical
half. Claws brown with black tips.
Wings. Forewings short, broad, membranes hyaline, darkened around apical margin in some specimens. C tan, R⫹Sc brown, R black within basal cell.
Other veins brown except CuA and CuP tan. Crossveins ra2-rp and rp-m1 not infuscate to moderately
infuscate, veins RA1 and RA2 thickened in majority of
specimens. Anterior two thirds or more of basal cell
tan. Eight apical cells. Clavus tan to orange-tan. Hind
wing membranes hyaline, wing veins brown except
CuA and CuP tan. Six apical cells. Plaga white.
Abdomen. Dorsal surface black with very Þne white
and gold hairs. Timbal covers brown, black in rare
exceptions. Lateral margins of tergites pruinose as well
as the following areas: I with two spots mesal to timbal
covers, trace of a spot centrally; II with large spot at
center of anterior margin; III with spot at center of
anterior margin, also a narrow band along anterior
border, extending two-thirds the distance from lateral
margin to the midline; IVÐVII with central spots decreasing in size caudally; VIII pruinose on anterior
half. Pygofer black. Sterna dark brown anteriorly, light
brown posteriorly, entirely pruinose. Opercula tan,
entirely pruinose in fresh specimens. Sternite VII tan,
slightly emarginate caudally, VIII tan, pinched, narrowly notched at caudal margin.
Male Terminalia. Uncus slightly attenuate (neotype) to triangular, shining black. Anal style tan.
Claspers with short, blunt processes and a square medial notch (Fig. 1A).
Female. Similar in structure and coloration to male
except for the following. Abdominal tergite II with a
pair of pruinose spots conßuent with those on I. Sternite VII with 90⬚ notch along caudal border, the pos-
818
ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA
terolateral corners rounded, bearing a pair of diffuse
brown spots.
Measurements. Males (n ⫽ 21). Body length: 32.5Ð
39.6, 36.9 ⫾ 1.9; forewing length: 36.1Ð 46.0, 41.6 ⫾ 2.3;
forewing width: 14.3Ð19.8, 17.5 ⫾ 1.3; head width:
11.9 Ð14.8, 13.3 ⫾ 0.7; pronotum width: 13.2Ð16.8,
14.9 ⫾ 0.9; mesonotum width: 11.0 Ð13.8, 12.7 ⫾ 0.8.
Females (n ⫽ 10). Body length: 29.2Ð37.1, 33.7 ⫾ 2.4;
forewing length: 35.9 Ð 45.2, 41.6 ⫾ 2.6; forewing width:
15.4 Ð19.4, 17.5 ⫾ 1.4; head width: 11.9 Ð14.4, 13.2 ⫾ 0.7;
pronotum width: 13.2Ð16.6, 15.2 ⫾ 1.0; mesonotum
width: 11.6 Ð14.0, 12.9 ⫾ 0.7.
Discussion. T. dorsatus inhabits a wide variety of
open habitats, ranging from native prairie remnants to
roadsides to agricultural Þelds. It occurs with a broad
assemblage of other cicada species across its range. At
the neotype locality, T. dorsatus was syntopic with T.
auriferus (Say), and sympatric with, but separated by
habitat from the arboreal species T. linnei (Smith &
Grossbeck), T. lyricen (DeGeer), T. pronotalis Davis
(⫽T. marginalis (Say), and T. walkeri Metcalf) and T.
pruinosus (Say). Collection dates range from 11-VI
(Otero Co., CO; GMCS) to 26-X (Payne Co., OK;
EMOS).
Two synonyms are listed for T. dorsatus: Thopha
varia Walker 1850 and Fidicina crassa Walker 1858
(reviewed in Davis 1915). WalkerÕs original descriptions do not explicitly comment on the characters I
concluded separate T. dorsatus from its cryptic species
(see diagnosis). Hemiptera curator Mick Webb (personal communication) located the material representing both of WalkerÕs synonyms in the Natural History
Museum (London, United Kingdom) and indicated all
have brown timbal covers and an entirely black tergum. I therefore retain both T. varia and F. crassa as
synonyms of T. dorsatus.
Davis (1915) (pl. 12; Þg. 1) published a photograph
of a male Tibicen dorsatus from Labette Co., KS. The
contrasting colors of C and R⫹Sc conÞrm that specimen is a true T. dorsatus, as does the line drawing of
the genitalia, showing short processes on the claspers.
Furthermore, Labette Co., in southeastern KS, is east
of the range of the new species. Lawson (1920) (p. 329,
pl. xx; Þgs. 5Ð 6) also described and Þgured the genitalia of true T. dorsatus. The posterior view of the
genitalia clearly shows claspers with blunt processes
and a square medial notch.
Tibicen tremulus sp. n
(Figs. 1B [male genitalia], 2B [habitus], 4AÐC [song],
5 [distribution]).
Description. HOLOTYPE: 1 male, USA, CO, Baca
Co., Picture Canyon Picnic Area, Comanche National
Grassland, 37.0119⬚ N, 102.7445⬚ W, 1,293 m, 11Ð12VIII-2007, specimen PC07-01, J. A. Cole. PARATYPES:
11 males, same data as holotype; 12 males, 2 females,
USA, KS, Seward Co., Jct. V Rd. and SR 54, 37.1697⬚ N,
100.7350⬚ W, 843 m, 13-VIII-2007, J. A. Cole.
Head. Slightly wider than anterior margin of
pronotum, covered with coarse white hairs. Rostrum
brown with black tip, extending caudally to metatho-
Vol. 101, no. 5
racic basisternum. Anteclypeus brown medially, black
anteriorly. Postclypeus brown, tan medially, transverse grooves dark brown, Þlled with coarse white
hairs, quite densely in many specimens. Lora black,
fading to brown anteriorly. Genae tan. Supra-antennal
plates brown ventrally with black stripe along anterior
margin from eye to postclypeus, entirely brown dorsally. Antennae brown, darker dorsally. Frons and
dorsal surface of postclypeus tan, forming a diamond
extending caudally to median ocellus. Vertex brown,
a black band between eyes, discontinuous in some
specimens. Brown stripes encroach anteriorly into
black band along Þssures lateral to each lateral ocellus
and medially to median ocellus.
Thorax. Pronotal collar brown except lateral margins of collar trimmed with black. Within collar, black
with following areas brown: a middorsal stripe conßuent anteriorly with collar, two small anteromedial
spots mesal to paramedian Þssures, conßuent with
collar in some specimens, two large lateral spots occupying lateral two thirds of pronotum. Mesonotum
background black. A pair of tan J-shaped marks originate at pronotal collar on the middorsal line, extend
posteriorly onto scutum, bend laterally and anteriorly around posterior border of parapsidial suture
and then widen caudally to contact anterior arms of
cruciform elevation. Often a small to large pruinose
spot at anterior conßuence of J-marks on middorsal
line. Lateral sigilla with two narrow to wide redbrown oblique stripes extending anterolaterally
from wide ends of J-marks to anterolateral corners
of scutum. A pair of pruinose spots extends posterolaterally along the parapsidial sutures from collar to
wide end of J-marks, often partially obscuring them.
Lateral margins of mesonotum with heavy pruinose
bands. Scutellum brown, anterior arms of cruciform
elevation black apically, enclosing a large pruinose
diamond-shaped spot anteriorly, which in some
specimens extends anteriorly to connect with pruinose spot behind collar at midline. Posterior arms
of cruciform elevation enclose pruinose spots laterally. Wing grooves brown, heavily pruinose. Metathoracic basisternum sooty, remainder of sterna
tan to brown, covered with dense pruinosity. Pleura
black, heavily pruinose.
Legs. Coxae tan with blackish apical spots. Trochanters tan basally, becoming brown apically, with
smoky longitudinal patches. Femora brown, carinae of
forefemoral ßexor surfaces smoky, spines dark brown.
Tibiae brown. Metatibiae with black tibial combs, variable number of dark brown spurs on apical half. Claws
brown with black tips.
Wings. Fore wings short, broad, membranes hyaline. C, R⫹Sc, CuA, CuP tan, R brown to blackish
within basal cell. Remaining veins dark brown. Crossveins ra2-rp and rp-m1 not infuscate to moderately
infuscate, RA1 and RA2 thickened in the majority of
specimens. Anterior two thirds or more of basal cell
tan. Eight apical cells. Clavus orange. Hind wing veins
tan from base to node, brown apically. Six apical cells.
Plaga white.
September 2008
COLE: A NEW CRYPTIC SPECIES OF Tibicen
Abdomen. Basal tergites black, posterior tergites
fading to reddish brown beginning at tergite V. Timbal
covers black. Lateral margins of tergites pruinose as
well as the following areas: I with wide spots centrally
and laterally; II with heavy spot on anterior midline; III
with central spot, also long anterolateral triangles or
stripes of varying development, usually extending
from lateral margins to three fourths the distance to
midline; IVÐVI with small central spots; VII sometimes
with anterolateral triangles; VIII pruinose on anterior
half. Pygofer black anteriorly and centrally, brown
laterally. Sterna dark brown anteriorly, light brown
posteriorly, pruinose. Sternite VIII tan, pinched and
narrowly notched caudally. Opercula tan, covered
with heavy pruinescence.
Male Terminalia. Uncus slightly attenuate (holotype) to triangular, reddish brown with black infuscations. Anal style tan basally, dark apically. Claspers
with processes long, attenuate, meeting medially in an
acute notch (Fig. 1B).
Female. Similar in structure and coloration to male
except for the following. Abdominal tergite II with a
pair of dorsolateral pruinose spots conßuent with
those on tergite I. Tergite IX tan with black dorsolateral stripes. Sternite VII with a 90⬚ notch along caudal
border, the posterolateral corners rounded, bearing a
pair of diffuse brown spots.
Measurements. Males (n ⫽ 26). Body length: 26.5Ð
38.6, 35.8 ⫾ 2.5; forewing length: 37.4 Ð 45.8, 42.5 ⫾ 1.9;
forewing width: 15.7Ð19.3, 17.2 ⫾ 0.8; head width:
12.8 Ð14.9, 13.9 ⫾ 0.4; pronotum width: 13.6 Ð16.1,
15.0 ⫾ 0.6; mesonotum width: 11.3Ð13.8, 12.8 ⫾ 0.6.
Females (n ⫽ 4). Body length: 30.6 Ð36.0, 32.8 ⫾ 2.5;
forewing length: 40.6 Ð 47.0, 42.8 ⫾ 2.9; forewing width:
16.0 Ð19.2, 17.5 ⫾ 1.5; head width: 12.9 Ð14.6, 13.8 ⫾ 0.7;
pronotum width: 14.0 Ð16.0, 14.9 ⫾ 0.9; mesonotum
width: 12.0 Ð13.7, 12.8 ⫾ 0.7.
Etymology. This speciÞc epithet is the Latin word
meaning “trembling, quaking, quivering, tremulous.”
The name describes the quality of the calling song to
human ears, and also refers to the rapid undulation of
the abdomen of a singing male.
Discussion
I examined T. dorsatus material from six museum
collections and determined 27% of the specimens represent T. tremulus. Although it does not seem to be
rare, T. tremulus is perhaps only locally abundant.
Some evidence suggests T. tremulus may have narrower ecological requirements than T. dorsatus. I
found them associated with sand sage (Artemisia filifolia Torr.) and soapweed yucca (Yucca glauca Nutt.)
at the holotype and paratype localities. Labels of several museum specimens indicate sandy habitats: KS,
Reno Co., sand dunes, Medora (1 male, MEKS); CO,
Prowers Co., sand dunes south of fairgrounds, U.S.
287/385, Lamar (2 males, GMCS); CO, Bent Co., sand
dunes, Rd. GG and Rd. 25 (1 female, GMCS). Davis
(1926) (p. 178, pl. XXI; Þg. 2) described and Þgured a
heavily pruinose specimen that is probably a T. tremu-
819
Fig. 2. Habitus of adult males illustrating diagnostic color
pattern features. (A) T. dorsatus. (B) T. tremulus sp. n.
lus from sand hills with sagebrush south of Lamar, CO
(Prowers Co.).
At the paratype locality, individuals perched on
yucca stalks where they were camoußaged among the
empty capsules. I collected Tibicen tremulus together
with T. dealbatus (Davis) and T. dorsatus at the type
locality, and with T. auriferus at the paratype locality.
Collection dates range from 13-VI (Caddo Co., OK;
EMOS) to 14-IX (Seward Co., KS; SEMK).
Diagnosis. Males of T. dorsatus and T. tremulus share
a triangular uncus with several other Tibicen, and
among these species T. dealbatus and T. pronotalis are
most similar (see key and Þgures in Lawson 1920). T.
dealbatus and T. pronotalis have clearly deÞned brown
bands at the apex of the abdominal tergites, which are
absent in T. dorsatus and T. tremulus. Tibicen pronotalis
lacks the prominent middorsal row of pruinose spots.
A row of middorsal spots may be present in T. dealbatus, but not normally developed to the degree seen
in T. dorsatus or T. tremulus. Habitats also differ, with
T. dorsatus and T. tremulus inhabiting herbaceous vegetation, whereas T. dealbatus and T. pronotalis are
arboreal.
Morphological characters separating T. dorsatus and
T. tremulus are found in Figs. 1 and 2. The shape of the
claspers (Fig. 1) distinguishes the males. The claspers,
normally hidden within the pygofer, may be exposed
by prying sternite VIII ventrally. Short blunt processes
and a square medial notch are diagnostic of T. dorsatus (Fig. 1A). The claspers of T. tremulus have
long, attenuate processes and an acute medial notch
(Fig. 1B).
820
ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA
Vol. 101, no. 5
Fig. 3. Calling song of T. dorsatus, topotype male, Atchison Co., KS. (A) Oscillogram of entire song. (B) Oscillogram of
1-s interval of main portion of calling song. (C) Spectrogram, same 1-s interval as in shown in B.
The color pattern characters (Fig. 2) separate a
large proportion of preserved specimens, but their
utility is limited by preservation quality and specimen
age. Males may be distinguished by the color of the
timbal covers, which are brown in T. dorsatus (Fig.
2A) and black in T. tremulus (Fig. 2B). Two males from
Cherokee Co., OK (GMCS), were the only exceptions
I encountered. Both have black timbal covers, but
the genitalia and wing vein coloration identify them
as T. dorsatus. Vein R⫹Sc in the forewing is dark
brown in T. dorsatus, contrasting with the tan C
(Fig. 2A), but in T. tremulus both C and R⫹Sc are
uniformly tan (Fig. 2B). This character is applicable
to both sexes but is difÞcult to use in old specimens,
because in T. dorsatus the darker R⫹Sc vein fades.
A reddish brown tinge on the posterior abdominal
tergites of T. tremulus is apparent in live and fresh
specimens, but in T. dorsatus the black on the tergites eventually fades and approaches the condition
in T. tremulus.
Song Analysis and Behavioral Observations. Recordings of topotype males from Atchison Co., KS,
assign the rattling song to T. dorsatus. Recordings of
males from Douglas Co., KS, were not signiÞcantly
different from topotype Atchison males in any song
parameter (all P values ⬎0.28; GLM), so I combined
recordings from these two localities in the following
analysis. The rattling song consists of three phrases
(Fig. 3A), throughout which a uniform syllable type of
period 26.0 ⫾ 1.1 ms is repeated at a rate of 38.9 ⫾ 1.7
s⫺1 (n ⫽ 12) (Fig. 3B). The Þrst phrase of the song is
an amplitude increase lasting 5.7 ⫾ 1.4 s, frequency
range 2.7Ð7.3 kHz (n ⫽ 7). Expansion of the male
abdomen accompanies this amplitude increase, a behavior that matches the resonant frequency of the
abdominal air sacs with that of the timbals (Pringle
1954). The main phrase is produced at maximum amplitude and lasts for 17.6 ⫾ 4.4 s, during which the
frequency range expands to 2.6 Ð12.7 kHz (n ⫽ 12)
(Fig. 3C). Principal energy lies between 2.9 and 7.4
kHz (Fig. 3C), and the frequency at maximum amplitude is 4.0 ⫾ 0.3 kHz (n ⫽ 12). The Þnal phrase of
the song is an amplitude decrease with frequencies
ranging from 2.8 to 8.3 kHz. The Þnal phrase lasts 5.1 ⫾
2.6 s (n ⫽ 3) in stationary males, but this portion is
truncated in males that use sing-ßy behavior or are
September 2008
COLE: A NEW CRYPTIC SPECIES OF Tibicen
821
Fig. 4. Calling song of T. tremulus sp. n., Baca Co., CO. (A) Oscillogram of entire song. (B) Oscillogram of 1-s interval
of main portion of calling song. (C) Spectrogram, same 1-s interval as in shown in B.
disturbed. Males most commonly produced one call
per location before ßying, but I observed one male in
Douglas Co., KS, that produced three bouts of song
from a single location without interruption. Singing
occurs from late morning until sundown, with increased activity in mid afternoon during the hottest
part of the day.
The trembling song belongs to the new species T.
tremulus, and the following data are based on recordings of Þve males from the type locality. Two phrases
occur in the song (Fig. 4A): a phrase consisting of a
uniform low amplitude band of frequencies ranging
from 3.9 to 5.8 kHz, and high amplitude phrase within
which the amplitude and frequency of the syllables are
modulated. Throughout the song, syllables with a period of 62.3 ⫾ 2.5 ms are repeated at a rate of 16.2 ⫾
0.6 s⫺1 (Fig. 4B). The frequency at maximum amplitude is 5.4 ⫾ 0.3 kHz. The modulations last 19.7 ⫾ 2.7
ms (Fig. 4B), during which amplitude increases and
the frequency range broadens to 3.6 Ð7.7 kHz (Fig.
4C). During the 43.2 ⫾ 5.8-ms intervals between modulations, the frequency range is 3.9 Ð5.9 kHz (Fig. 4C),
similar to that of the unmodulated phrase. The modulated phrase lasts ⬇22.8 s, as measured from one
complete song (Fig. 4A).
During modulation, male T. tremulus rapidly undulate the abdomen in the dorsoventral plane. Such
abdominal movements modulate amplitude and frequency by altering the curvature and tension of the
timbal membranes (Pringle 1954). Several Tibicen
modulate their songs with abdominal movements,
including T. superbus (Fitch) (see Sanborn and
Phillips 2004), T. dealbatus, and T. pronotalis. Abdominal movements are not made by singing male T.
dorsatus.
Calling in T. tremulus lasted from late morning until
dusk at the type locality. Peak acoustic activity occurred between 1000 and 1100 hours and again from
1400 to 1600 hours. Recordings were made between
1400 and 1600 hours. T. tremulus and T. dorsatus males
called together in the same microhabitats at the
same times. I observed one male of each species on
the same bush, alternately chorusing with males of
their respective species. As in T. dorsatus, male T.
tremulus rarely produce more than one call from any
single location.
Male T. tremulus produce a courtship song in the
presence of a female. The courtship song was not
recorded, but it is qualitatively similar to the unmodulated phrase of the calling song, although it may be
822
ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA
Vol. 101, no. 5
Fig. 5. Distribution estimated from museum specimens. Gray circles, T. dorsatus; black triangles, T. tremulus sp. n.
produced at lower amplitude. Male T. dorsatus lack
such behavior. To the contrary, a Douglas Co., KS,
male was observed backing down a sunßower stem
toward a female while producing the full-amplitude
calling song.
The literature contains qualitative descriptions of
the songs of both species. Beamer (1929) (p. 219)
likened the song of T. dorsatus to “the distant hum of
a mowing machine or certain type of tractor.” His
description calls to mind the rattling song of true T.
dorsatus. Beamer made his observations three miles
west of Lawrence, KS, where true T. dorsatus is common. Tinkham (1941) (p. 173) described the song of
T. dorsatus from Texas to be “piercing like a steam
whistle.” This description accurately describes the
shrill character of the T. tremulus song, and a museum
record shows the new species occurs in northern
Texas.
Distribution. T. dorsatus is widespread in the prairie
biome of the United States (Fig. 5). This species is
common in the eastern Great Plains in areas formerly
supporting tallgrass prairie habitat. A single T. dorsatus
male in EMUM labeled AL, Lee Co., 3-V-1987, Samir
F. was not included in Fig. 5. This record is a signiÞcant
outlier in terms of geography, habitat, and emergence
date and requires veriÞcation.
Records show that T. tremulus inhabits a subset of
the western range of T. dorsatus (Fig. 5). The distribution of T. tremulus coincides with shortgrass prairie
habitats in the western Great Plains. A female from
Ponca City, Kay Co., OK at longitude ⫺97.08⬚ (EMOS)
represents the easternmost record for the new species.
More collecting is needed in the northern Great Plains
(Nebraska, IA, and the Dakotas), New Mexico, and
Texas to clarify the northern and southern limits of T.
tremulus. In addition to my observations at the type
locality, identical labels on museum specimens provide more evidence that the two species are both
sympatric and synchronic. Both species were collected together at the same locality and date on two
occasions: CO, Otero Co., Hwy. 109, mile post 33 (1
male of each species, 11-VIII-1990, B. Kondratieff, D.
Leatherman; GMCS), and KS, Barber Co., Medicine
Lodge (1 male and 1 female of each species, 16-VIII1951, W. R. Enns; EMUM).
Conclusions and Future Directions. T. tremulus is a
cryptic species that has been confused with T. dorsatus
for ⬎180 yr. Analysis of calling songs led to the discovery of two sympatric species distinguished by male
genitalia and color pattern characters. Although Tibicen tremulus and T. dorsatus are cryptic species they
may not be sibling species. In contrast, there is strong
color pattern resemblance between the two species.
However, T. tremulus, T. dealbatus, and T. pronotalis all
have similar clasper morphologies, and all three produce songs with amplitude and frequency modulation.
Perhaps similar color patterns evolved independently,
possibly to camoußage the cicadas among their shared
habitat of dry herbaceous vegetation. A phylogenetic
study of Tibicen that subjects these conßicting characters to a congruence test may lead to interesting
conclusions concerning behavioral, ecological, and
morphological evolution.
Acknowledgments
I thank: Will ChatÞeld-Taylor for specimen photography
and collecting assistance, Michael GreenÞeld for loaning the
recording equipment, and Cornelia Becker and Monica
Papes for help with GIS mapping. Daphne Fautin reviewed
the manuscript and provided input with ICZN issues. Two
anonymous reviewers provided valuable comments. Ginger
Miller commented on the revised manuscript. Specimens
were examined courtesy of Don Arnold (EMOS), Zach Falin
and Jennifer Thomas (SEMK), Boris Kondratieff (GMCS),
Ed Riley (TAMU), Kristin Simpson (EMUM), and Gregory
Zolnerowich (MEKS).
September 2008
COLE: A NEW CRYPTIC SPECIES OF Tibicen
References Cited
Alexander, R. D. 1957. The taxonomy of the Þeld crickets of
the eastern United States (Orthoptera: Gryllidae:
Acheta). Ann. Entomol. Soc. Am. 50: 584Ð602.
Beamer, R. H. 1929. Studies on the biology of Kansas Cicadidae. Univ. Kans. Sci. Bull. 18: 155Ð263.
Bickford, D., D. J. Lohman, N. S. Sodhi, P.K.L. Ng, R. Meier,
K. Winker, K. K. Ingram, and I. Das. 2006. Cryptic species as a window on diversity and conservation. Trends
Ecol. Evol. 22: 148Ð155.
Cornell Lab of Ornithology. 2007. Raven Lite computer
program, version 1.0. Cornell Lab of Ornithology,
Ithaca, NY.
Davis, W. T. 1915. A new variety of cicada resembling C.
dorsata. J. N Y Entomol. Soc. 23: 161Ð164.
Davis, W. T. 1926. New cicadas from California and Arizona
with notes on several other species. J. N Y Entomol. Soc.
34: 177Ð190.
Davis, W. T. 1941. New cicadas from North America with
notes. J. N Y Entomol. Soc. 49: 85Ð96.
Davis, W. T. 1944. The remarkable distribution of an American cicada: a new genus, and other cicada notes. J. N Y
Entomol. Soc. 52: 213Ð222.
ESRI 2006. ArcGIS computer program, version 9.2. ESRI,
Redlands, CA.
Froeschner, R. C. 1952. A synopsis of the Cicadidae of Missouri (Homoptera). J. N Y Entomol. Soc. 60: 1Ð13.
Heath, J. E., and A. F. Sanborn. 2007. A new species of the
genus Okanagana (Hemiptera: Cicadoidea: Cicadidae)
from Arizona. Ann. Entomol. Soc. Am. 100: 483Ð 489.
Kondratieff, B. C., A. R. Ellingson, and D. A. Leatherman.
2002. Insects of Western North America 2. The Cicadas
of Colorado (Homoptera: Cicadidae, Tibicinidae). Department of Bioagricultural Sciences and Pest Management, Colorado State University, Fort Collins, CO.
Lawson, P. B. 1920. The Cicadidae of Kansas. Kans. Univ.
Sci. Bull. 12: 309 Ð352.
Marshall, D. C., and J. R. Cooley. 2000. Reproductive character displacement and speciation in periodical cicadas,
with description of a new species, 13-year Magiciada
neotredecim. Evolution 54: 1313Ð1325.
Minitab Inc. 2000. Minitab statistical software computer
program, version 13. Minitab Inc., State College, PA.
823
Moulds, M. 2005. An appraisal of the higher classiÞcation of
cicadas (Hemiptera: Cicadoidea) with special reference
to the Australian fauna. Rec. Aust. Mus. 57: 375Ð 446.
Pettersson Elektronik AB. 2001. Bat Sound Pro computer
program, version 3.3. Pettersson Elektronik AB, Uppsala,
Sweden.
Pringle, J.W.S. 1954. A physiological analysis of cicada song.
J. Exp. Biol. 31: 525Ð560.
Sanborn, A. F. 1997. Body temperature and the acoustic
behavior of the cicada Tibicen winnemanna (Homoptera:
Cicadidae). J. Insect Behav. 10: 257Ð264.
Sanborn, A. F., and P. K. Phillips. 2004. Neotype and allotype description of Tibicen superbus (Hemiptera: Cicadomorpha: Cicadidae) with description of its biogeography
and calling song. Ann. Entomol. Soc. Am. 97: 647Ð 652.
Say, T. 1825. Descriptions of new Hemipterous insects collected in the expedition to the Rocky Mountains, performed by order of Mr. Calhoun, Secretary of War, under
command of Major Long. J. Natl. Acad. Sci. Phila. 6:
235Ð244.
Sueur, J., and S. Puissant. 2007. Similar look but different
song: a new Cicadetta species in the montana complex
(Insecta, Hemiptera, Cicadidae). Zootaxa 1442: 55Ð 68.
Tinkham, E. R. 1941. Biological and faunistic notes on the
Cicadidae of the Big Bend Region of Trans-Pecos Texas.
J. N Y Entomol. Soc. 49: 165Ð182.
Van Duzee, E. P. 1916. Check list of the Hemiptera (excepting the Aphididae, Aleurodide and Coccidae) of
America, North of Mexico. New York Entomological Society, New York.
Walker, T. J., J. J. Whitesell, and R. D. Alexander. 1973. The
robust conehead: two widespread sibling species (Orthoptera: Tettigoniidae: Neoconocephalus“robustus”). Ohio J.
Sci. 73: 321Ð330.
Walker, T. J., T. G. Forrest, and J. D. Spooner. 2003. The
rotundifolia complex of the genus Amblycorypha (Orthoptera: Tettigoniidae): songs reveal new species. Ann.
Entomol. Soc. Am. 96: 433Ð 447.
Wells, M. M., and C. S. Henry. 1998. Songs, reproductive
isolation, and speciation in cryptic species of insects, pp.
217Ð233. In D. J. Howard and S. H. Berlocher [eds.],
Endless forms: species and speciation. Oxford University
Press, New York.
Received 16 November 2007; accepted 16 May 2008.