Revista de Biología Tropical, ISSN: 2215-2075, Vol. 73 (S2): e64519, mayo 2025 (Publicado May. 15, 2025)

Acoustic and morphological differences in Colinus genus

(Galliformes: Odontophoridae) support the occurrence of four species

Luis Sandoval1, 2 *; https://orcid.org/0000-0002-0793-6747

Gilbert Barrantes3; https://orcid.org/0000-0001-8402-1930

Eric J. Fuchs3; http://orcid.org/0000-0002-6645-9602

Diego Ocampo2, 4; https://orcid.org/0000-0002-7411-2027

1. Laboratorio de Ecología Urbana y Comunicación Animal, Escuela de Biología, Universidad de Costa Rica, San José,

Costa Rica; biosandoval@gmail.com (*Correspondencia).

2. Colección de Ornitología, Museo de Zoología, CIBET, Universidad de Costa Rica, San José, Costa Rica.

3. Escuela de Biología, Universidad de Costa Rica, San José, Costa Rica; gilbert.barrantes@gmail.com;

e.j.fuchs@gmail.com

4. Museum of Natural Science, Louisiana State University, Baton Rouge LA, 70803 USA; docampo@lsu.edu

Received 31-VIII-2024. Corrected 22-I-2025. Accepted 04-III-2025.

ABSTRACT

Introduction: The taxonomy of Galliformes species, a group closely associated with humans since antiquity,

remains unclear at various taxonomic levels, producing taxonomic changes constantly.

Objective: Our objective is to provide morphological and acoustic data to support the recent taxonomic rec-

ognition of Colinus leucopogon (Spot-bellied Bobwhite) as a distinct species from Colinus cristatus (Crested

Bobwhite).

Methods: Using a combination of morphological and acoustic analyses, we assessed the differences between

these two recently recognized species and compared them with the two other well-established species within the

genus: C. nigrogularis (Black-throated Bobwhite) and C. virginianus (Northern Bobwhite).

Results: Our acoustic analysis of male songs from 64 individuals showed significant differences in maximum

amplitude frequency, song duration, and number of elements, which can act as a reproductive barrier between

C. cristatus and C. leucopogon. Morphological analyses, however, revealed only limited differences, primarily in

tarsus length and wing chord length.

Conclusions: Our findings suggest that while male song characteristics strongly support the recognition of C.

cristatus and C. leucopogon as distinct species, morphological differences are less pronounced, potentially due to

ecological factors such as habitat similarity and altitudinal distribution. This study highlights the importance of

including both acoustic and morphological traits in resolving taxonomic uncertainties and understanding species

boundaries in Galliformes.

Key words: vocal differences; morphology variation; quail; reproductive barriers; taxonomy.

RESUMEN

Diferencias acústicas y morfológicas apoyan la presencia de cuatro especies del género Colinus

(Galliformes: Odontophoridae)

Introducción: La taxonomía de las especies de Galliformes, un grupo estrechamente asociado con los humanos

desde la antigüedad, sigue siendo poco clara en varios niveles taxonómicos.

https://doi.org/10.15517/rev.biol.trop..v73iS2.64519

SUPPLEMENT

SECTION: ACOUSTICS

2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 73 (S1): e64519, mayo 2025 (Publicado May. 15, 2025)

INTRODUCTION

Galliformes species have been closely asso-

ciated with humans since antiquity, yet their

taxonomy remains highly confusing at vari-

ous levels (Carroll, 1994; Cracraft et al., 2004;

Delacour, 1949; Fain & Houde, 2004; Groth

& Barrowclough; 1999, Holman, 1961; Madge

& McGowan, 2002; McGowan & Panchen,

1994; Salter et al., 2022; Sibley & Ahlquist,

1990). The limits that define species within this

group are unclear, and the characteristics used

to distinguish between species are associated

with allopatric distributions and male plumage

variation, across species (Carroll, 1994; Madge

& McGowan, 2002). As a result, the number

of recognized species in some genera, such as

Lophura (Phasianidae), Lagopus (Phasianidae),

and Colinus (Odontophoridae), differs among

authors (American Ornithologists’ Union

[AOU], 1983; AOU, 1998; Carroll, 1994; Dela-

cour, 1949; Hellmayr & Conover, 1942; Madge

& McGowan, 2002; Stiles & Skutch, 1989).

Within the genus Colinus, the number of

recognized species ranges from three (AOU,

1983; AOU, 1998; Hellmayr & Conover, 1942)

to four (Carroll, 1994; Chesser et al., 2024; Gill

et al., 2024; Madge & McGowan, 2002; Stiles &

Skutch, 1989), with 45 subspecies recognized in

a super-species complex (Carroll, 1994; Madge

& McGowan, 2002). When only three species

are recognized, C. cristatus (Crested Bobwhite)

and C. leucopogon (Spot-bellied Bobwhite)

are often grouped together as Crested Bob-

white (AOU, 1983, AOU, 1998; Garrigues &

Dean, 2014; Hellmayr & Conover, 1942). This

grouping was initially proposed by Hellmayr &

Conover (1942) and subsequently supported by

the AOU (1983) AOU (1998). They argued that

the plumage differences between the Central

American (C. leucopogon) and South American

(C. cristatus) forms are continuous (Hellmayr

& Conover, 1942). In contrast, when C. leuco-

pogon and C. cristatus are recognized as two

distinct species, the separation is based on

differences in male and female crest size, plum-

age, and color patterns (Carroll, 1994; Madge

& McGowan, 2002; Stiles & Skutch, 1989) and

supported by genetic reciprocally monophyly

(Salter et al., 2022). But, no formal morphologi-

cal analyses have been done in order to stablish

the degree of morphological variation between

these groups as a way to delineate species limits.

Acoustic analysis in mating signals is

another approach that might produce reli-

able information to clarify the species status

of C. leucopogon (Price, 1998; Slabbekoorn &

Smith, 2002; West-Eberhard, 1983). The male

bobwhite song attracts females and deter males

(Sandoval, 2011b), and in C. leucopogon male

Objetivo: Nuestro objetivo es proporcionar datos morfológicos y acústicos para apoyar el reciente reconoci-

miento taxonómico de Colinus leucopogon (Codorniz ventrinegro) como una especie distinta de Colinus cristatus

(Codorniz crestado).

Métodos: Utilizando una combinación de análisis morfológicos y acústicos, evaluamos las diferencias entre estas

dos especies recientemente reconocidas y las comparamos con las otras dos especies bien establecidas dentro del

género: C. nigrogularis (Codorniz garganta negra) y C. virginianus (Codorniz norteño).

Resultados: Nuestro análisis acústico de los cantos de los machos de 64 individuos mostró diferencias significa-

tivas en la frecuencia de amplitud máxima, la duración del canto y el número de elementos, lo que puede actuar

como una barrera reproductiva entre C. cristatus y C. leucopogon. Los análisis morfológicos, sin embargo, revela-

ron solo diferencias limitadas, principalmente en la longitud del tarso y la longitud de la cuerda alar.

Conclusiones: Estos hallazgos sugieren que, si bien las características del canto de los machos respaldan firme-

mente el reconocimiento de C. cristatus y C. leucopogon como especies distintas, las diferencias morfológicas son

menos pronunciadas, posiblemente debido a factores ecológicos como la similitud del hábitat y la distribución

altitudinal. Este estudio destaca la importancia de incluir tanto los rasgos acústicos como los morfológicos para

resolver las incertidumbres taxonómicas y comprender los límites entre las especies de Galliformes.

Palabras clave: barreras reproductivas; diferencias vocales; codorniz; taxonomía; variación morfológica.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 73 (S2): e64519, mayo 2025 (Publicado May. 15, 2025)

song plays an important role in sexual selection

(Sandoval, 2008, Sandoval, 2011a; Sandoval

& Barrantes, 2012). Divergence in song traits

could act as a reproductive barrier between

species, potentially through female species rec-

ognition, increasing reproductive isolation (de

Kort et al., 2002; Irwin, 2000; Irwin et al., 2001).

Furthermore, male song in bobwhites is geneti-

cally determined (Catchpole & Salter, 2008;

Kroodsma, 2004; Konishi, 1963), and in species

lacking song learning ability (e.g., Galliformes),

song variation has been used as a criterion to

delineate species limits (Irwin et al., 2001; Isler

et al., 1999; Isler et al., 2005; Isler et al., 2007;

Seddon, 2005).

Our objective is to use morphological

and acoustic data to test whether the recent

taxonomic recognition of C. leucopogon is

a distinct species from C. cristatus (Crested

Bobwhite). We predict that if morphology and

songs serve as distinguishing traits for separat-

ing C. leucopogon from C. cristatus, the dif-

ferences in these traits should be comparable

to or greater than those observed between C.

nigrogularis (Black-throated Bobwhite) and C.

virginianus (Northern Bobwhite), which have

long been recognized as distinct species (AOU,

1998; Madge & McGowan, 2002).

MATERIALS AND METHODS

Acoustic Analysis: We analyzed WAV

recordings of male songs (Fig. 1) from vari-

ous sources, including the Cornell Macaulay

Sound Library, LS records, commercial audio

files (cassette or CD), and private collections

(Appendix 1). We used this vocalization restrict

to males, because are used for female attraction

and male-male interaction (Sandoval, 2011a;

Sandoval, 2011b; Sandoval & Barrantes, 2012).

In total, we analyzed recordings from 64 indi-

viduals from the four bobwhite groups: 10 C.

cristatus, 22 C. leucopogon, 8 C. nigrogularis,

and 22 C. virginianus. For each recording, we

randomly selected and analyze five songs. If

a recording contained five or fewer songs, all

songs were analyzed.

We conducted the song analysis using

Raven 1.6 (Cornell Lab of Ornithology, Ithaca,

NY, USA) with a combination of waveform

window for duration measurements and power

spectrum window for frequency measure-

ments. We used 30 dB threshold to select the

Fig. 1. Representative male song sonograms of the four Colinus quail species.

4Revista de Biología Tropical, ISSN: 2215-2075 Vol. 73 (S1): e64519, mayo 2025 (Publicado May. 15, 2025)

minimum and maximum frequency of the

songs in the power spectrum window. We uti-

lized the spectrogram window for song iden-

tification and selection, ensuring that songs

overlapping with other sounds in frequency

were excluded from the analysis. The following

settings were applied in Raven 1.6 to construct

the spectrogram window: a temporal resolu-

tion of 0.5 s, a frequency resolution of 2 kHz

with a Hann window, 256 kHz sampling, and

50% overlap. Songs recorded on cassette were

digitized at a sample rate of 44 100 Hz and

16-bit resolution using Cool Edit 2000 version

1.0 (Johnston, 1999) and saved in WAV format.

For each selected song, we measured two

groups of frequency and duration characteris-

tics. The first group described the entire song

and included: 1) duration (s); 2) minimum

frequency (Hz); 3) maximum frequency (Hz);

4) frequency of maximum amplitude (Hz); and

5) the number of elements in the song (discrete

parts of the song separated by time or frequen-

cy, Fig. 1). The second group focused on indi-

vidual elements within the song and included:

1) duration (s); 2) time between elements (s);

3) minimum frequency (Hz); 4) maximum

frequency (Hz); and 5) frequency of maximum

amplitude (Hz, Fig. 1).

We conducted discriminant function anal-

yses (DFA) to estimate which variables of the

song discriminate between male songs, follow-

ing methodologies used in previous studies that

employed acoustic characteristics to resolve

species differences (e.g., Cadena & Cuervo,

2010; Millsap et al., 2011; Sandoval et al., 2014;

Sandoval et al., 2017). In the first DFA, we

used the average of each song measurement

per recording as dependent variables, with spe-

cies name as the grouping variable. A second

DFA was conducted to compare male song

differences among species using all measure-

ments per element. In this DFA, we also used

the average of each song element per record-

ing as dependent variable and species name as

the grouping variable. We do not pool all the

measurements in a single DFA, because some

of the measurements in the entire song and ele-

ments were the same (i.e., maximum frequency

of the entire song and one of the elements),

and pooling measurement will count twice the

measurements. Both DFAs employed a back-

ward stepwise approach to select the minimum

number of song measurements that best dis-

tinguished the four bobwhite species. For both

analyses, measurements with the lowest F-value

were sequentially excluded, and the analysis

was rerun after each deletion. This procedure

was repeated until we obtained a model with

the fewest variables that provided the high-

est accuracy in species classification based on

the jackknife method. We conducted one-way

analyses of variance (ANOVA) as post-hoc tests

to compare the variation in song measurements

selected in each DFA across species.

Morphological Analysis: We measured

six morphological characteristics, including: 1)

tarsus length (from the intertarsal joint to the

middle of the sole of the foot), 2) wing chord

length (unflattened), 3) tail length, 4) cul-

men length, 5) culmen width, and 6) culmen

depth, from 225 adult individuals in museum

collections (Appendix 2). All measurements

were taken to the nearest 0.1 mm following

the methods described by Sandoval & Mennill

(2013). The sample included 89 C. cristatus

(38 females and 51 males), 92 C. leucopogon

(35 females and 57 males), 8 C. nigrogularis (3

females and 5 males), and 36 C. virginianus (14

females and 22 males).

We conducted two separate backward step-

wise DFA, one for each sex, to determine which

morphological measurements differed among

the four bobwhite species. As in previous DFAs,

we selected the minimum number of mor-

phological measurements that best separated

between the four species for each sex. Addi-

tionally, we performed ANOVA as post-hoc

tests to compare variation in the morphological

measurements selected in each DFA among the

species per sex.

RESULTS

We analyzed 271 songs from the four bob-

white species, with a mean (± SE) of 4.37 ± 1.01

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 73 (S2): e64519, mayo 2025 (Publicado May. 15, 2025)

songs per recording. All species’ songs included

two distinct elements (Fig. 1). Noticeable dif-

ferences were observed in the songs between

the four species. The best discriminant function

analysis (DFA) model, which is based on the

characteristics of the whole song, correctly clas-

sified 69 % of songs into their respective spe-

cies. This model included maximum amplitude

frequency, duration, and the number of ele-

ments (Wilk’s λ = 0.09, F9,125 = 25.85, P < 0.001,

Fig. 2). Maximum amplitude frequency (F3,58

= 13.45, P < 0.001) was significantly lower in

C. leucopogon and significantly higher in C.

cristatus, compared to the other two species,

for which maximum amplitude frequency was

similar (Fig. 3). Song duration (F3,58 = 5.18, P

= 0.003) was significantly shorter in the C. leu-

copogon than in the other three species (Fig. 3).

The number of elements per song (F3,58 = 13.03,

P < 0.001) was significantly higher in both C.

leucopogon and C. cristatus compared to the

other two species (Fig. 3).

The best DFA model based on measure-

ments of individual song elements correctly

classified 92 % of songs to the corresponding

species. This model included the maximum

amplitude frequency of the first and third

elements, minimum frequency, duration of

the first element, and time between elements

(Wilk’s λ = 0.007, F18,82 = 22.43, P < 0.001, Fig.

2). The maximum amplitude frequency of the

first song element (F3,34 = 8.13, P < 0.001) was

significantly higher in the C. cristatus (Fig. 4),

while the maximum amplitude frequency of the

third song element (F3,34 = 8.92, P < 0.001) was

significantly lower in the C. leucopogon (Fig. 4).

The duration of the first element (F3,34 = 6.98, P

< 0.001) and the time between elements (time

between elements 1 and 2: F3,34 = 118.81, P <

0.001; time between elements 2 and 1: F3,34 =

95.65, P < 0.001) were significantly longer in

the C. virginianus and C. nigrogularis (Fig. 4).

The minimum frequency of the third element

(F3,34 = 2.41, P = 0.08) did not significantly dif-

fer between species (Fig. 4).

Our analyses revealed that morphological

measurements varied across the four species in

both males and females. For females, the best

DFA model correctly classified 67 % of indi-

viduals to their respective species and included

Fig. 2. Plot of the first two discriminant functions for measurements of male solo song and each song element, and female

and male morphometric measurements between the four species of Colinus bobwhites (red: C. cristatus, green: C. leucopogon,

blue: C. virginianus, and grey: C. nigrogularis) based on the best model for each comparison.

6Revista de Biología Tropical, ISSN: 2215-2075 Vol. 73 (S1): e64519, mayo 2025 (Publicado May. 15, 2025)

tarsus length, wing chord length, and culmen

length (Wilk’s λ = 0.20, F9,187 = 22.32, P < 0.001,

Fig. 2). Tarsus length (F3,86 = 59.16, P < 0.001),

wing chord length (F3,86 = 18.37, P < 0.001),

and culmen length (F3,86 = 50.57, P < 0.001)

were significantly greater in the C. virginianus

and C. nigrogularis compared to the other two

species (Table 1).

For males, the best DFA model cor-

rectly classified 66 % of individuals to the

Fig. 3. Solo song characteristics (mean + SE) selected on the best model of discriminant function analysis for comparison of

the four Colinus species. Bars connected by different letters are significantly different in pairwise comparisons.

Table 1

Morphological measurements (mean ± SE) selected from the best model of discriminant function analysis for comparison

of the four Colinus species separated by sex. Species with different letters next to the measurement values are significantly

different in pairwise comparisons.

C. cristatus C. leucopogon C. nigrogularis C. virginianus

Males

Tarsus length 24.04 ± 0.25 (a) 23.15 ± 0.18 (b) 29.16 ± 0.81 (c) 29.55 ± 0.49 (c)

Wing chord 100.11 ± 0.79 (a) 99.57 ± 0.45 (a) 100.2 ± 3.1 (ac) 105.32 ± 1.25 (bc)

Tail length 56.67 ± 0.8 (a) 51.68 ± 0.63 (b) 48 ± 1.55 (b) 49.77 ± 1.21 (b)

Culmen length 12.83 ± 0.09 (a) 12.89 ± 0.1 (a) 15.05 ± 0.23 (b) 15.28 ± 0.17 (b)

Culmen depth 10.45 ± 1.61 8.4 ± 0.06 8.24 ± 0.27 8.23 ± 0.07

Females

Tarsus length 23.27 ± 0.28 (a) 22.5 ± 0.27 (a) 28.06 ± 0.7 (b) 29.2 ± 0.56 (b)

Wing chord 97.11 ± 0.77 (a) 97.23 ± 0.58 (a) 95 ± 4.58 (a) 107.14 ± 1.71 (b)

Culmen length 12.59 ± 0.11 (a) 12.33 ± 0.14 (a) 14.4 ± 0.45 (b) 15.07 ± 0.2 (b)

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 73 (S2): e64519, mayo 2025 (Publicado May. 15, 2025)

corresponding species and included tarsus

length, wing chord length, tail length, culmen

length, and culmen depth (Wilk’s λ = 0.15,

F15,333 = 22.96, P < 0.001, Fig. 2). Tarsus length

(F3,131 = 86.25, P < 0.001), wing chord length

(F3,131 = 7.74, P < 0.001), and culmen length

(F3,131 = 82.91, P < 0.001) were significantly

greater in the C. virginianus and C. nigrogularis

(Table 1). Tail length (F3,131 = 13.58, P < 0.001)

was significantly longer in the C. cristatus

(Table 1). Culmen depth (F3,131 = 0.93, P = 0.43)

was similar across all species (Table 1).

DISCUSION

We found that the differences in song

characteristics between C. leucopogon and C.

cristatus were greater, and showed no overlap

in our analysis, compared to the differences

and the overlap observed between C. virginia-

nus and C. nigrogularis, two species that have

long been recognized as distinct (AOU, 1998;

Madge & McGowan, 2002). Since male solo

songs in bobwhites play an important role

in sexual selection, including female attrac-

tion and male-male interactions (Sandoval,

2008, Sandoval, 2011b; Sandoval & Barrantes,

2012), our findings suggest that the significant

song divergence between C. leucopogon and C.

cristatus, historically grouped as a single spe-

cies on several occasions (AOU, 1983; AOU,

1998; Garrigues & Dean, 2014; Hellmayr &

Conover, 1942), may serve as a distinguishing

trait between both specie. These differences in

song are particularly important for taxonomic

considerations because male song in bobwhites

is genetically determined (Catchpole & Slater,

2008; Konishi, 1963; Kroodsma, 2004). In con-

trast, C. virginianus and C. nigrogularis exhib-

ited much greater similarity in their male song

characteristics. The song differences between

C. leucopogon and C. cristatus and similarity

between C. virginianus and C. nigrogularis may

be a consequence of the vegetation structure

where each species occur. For example, C. vir-

ginianus and C. nigrogularis inhabit pine forest

Fig. 4. Acoustic characteristics per element (mean + SE) based on the results on the best model of discriminant function

analysis for comparison of the four Colinus species. Species connected by different letters are significantly different in

pairwise comparisons.

8Revista de Biología Tropical, ISSN: 2215-2075 Vol. 73 (S1): e64519, mayo 2025 (Publicado May. 15, 2025)

and dense scrubs and grass-brushes (Madge &

McGowan, 2002), which have obstacle of larger

size for song transmission, and consequently

favoring shorter songs. Meanwhile, C. leuco-

pogon inhabit dry forest grassland that have tall,

thin grasses (Stiles & Skurch, 1989); vegetation

that will favor longer songs. But, C. cristatus

that inhabit grassland of humid forest, which

are denser in vegetation (Madge & McGowan,

2002), will favor the longer song of all four spe-

cies to transmit.

Morphological variation was associated

with the geographic distribution of the species

rather than differences between individual spe-

cies. Specifically, we found that C. virginianus

and C. nigrogularis were overall larger than C.

leucopogon and C. cristatus. Consequently, the

most pronounced morphological differences

were observed between the two species with

the northernmost distributions. This lack of

morphological differences between geographi-

cally closer pairs of species may be attrib-

uted to their use of similar habitats (Madge &

McGowan, 2002; Mayr, 1976; Ricklefs, 2012).

Both C. leucopogon and C. cristatus inhabit

tropical grasslands with isolated trees and small

forest patches (Madge & McGowan, 2002; Stiles

& Skutch, 1989), while C. virginianus and C.

nigrogularis occupy dry and temperate grass-

lands with small bushes (Madge & McGowan,

2002). Conversely, body size in closely related

species often varies according to latitude or

altitude, following Bergmann’s rule, where spe-

cies at higher latitudes or altitudes tend to have

larger body sizes (Gutiérrez-Pinto et al., 2014;

Meiri, 2011; Sandoval et al., 2014; Sandoval et

al., 2017). Our finding that the two species with

northern distributions had larger body sizes

is consistent with this expectation and it is a

pattern common among other groups of close-

ly related species of birds, such as Melozone

(Sandoval et al., 2014, Sandoval et al., 2017),

Pogoniulus (Sebastianelli et al., 2022), and Tyto

(Romano et al., 2021).

In conclusion, our study found that C. leu-

copogon and C. cristatus are fully distinguish-

able based on male solo song, a trait that is

important in sexual selection (Sandoval, 2008,

Sandoval, 2011a, Sandoval, 2011b; Sandoval &

Barrantes, 2012). The lack of significant mor-

phological differences between these species

may be due to ecological constraints, such as

those outlined by Bergmann’s rule, given their

similar habitats and altitudinal distributions

(Gutiérrez-Pinto et al., 2014; Meiri, 2011; San-

doval et al., 2014, Sandoval et al., 2017).

Ethical statement: the authors declare that

they all agree with this publication and made

significant contributions; that there is no con-

flict of interest of any kind; and that we fol-

lowed all pertinent ethical and legal procedures

and requirements. All financial sources are fully

and clearly stated in the acknowledgments sec-

tion. A signed document has been filed in the

journal archives.

See supplementary material

a01v73s2-suppl1

ACKNOWLEDGEMENTS

We thank the Museo de Zoología Universi-

dad de Costa Rica, the Field Museum of Natu-

ral History, and the Louisiana State University

Museum of Natural Science for access to speci-

mens of the study species; and to the Macaulay

Library of Natural Sounds, the Laboratorio de

Bioacústica Universidad de Costa Rica, and

David Ascanio for recordings. This investiga-

tion was supported by Vicerrectoría de Inves-

tigación under the grant number C2705 to LS.

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