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Rev. Biol. Trop. (Int. J. Trop. Biol.) • Vol. 69(1): 231-244, March 2021

Estimation of bat colony size even with low recapture rates:

an example based on the Cormack-Jolly-Seber model in Oaxaca, México

Antonio Santos-Moreno

& Itandehui Hernández-Aguilar

1. Laboratorio de Ecología Animal, Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional-

Unidad Oaxaca, Instituto Politécnico Nacional, México; asantosm90@hotmail.com

2. Departamento de Conservación de la Biodiversidad, El Colegio de la Frontera Sur, Unidad San Cristóbal, Chiapas,

México; itandehui0901@gmail.com

* Correspondence

Received 28-IV-2020. Corrected 17-X-2020. Accepted 19-XI-2020.

ABSTRACT. Introduction: Group or colony size is an important variable that is related to biological, ecologi-

cal, and conservation aspects of bats. However, estimating the size of each colony or group in roosts used by

more than one species is particularly difficult, especially when recapture rates are very low (< 10 %). Objective:

Estimate the colony size of 14 species of bats: one emballonurid, one natalid, four mormoopids, seven phyl-

lostomids, and one vespertilionid, which roosted throughout one year (July 2016 to June 2017) in a mine and

two caves -Cerro Huatulco and El Apanguito- in the Sierra Sur and Costa of the state of Oaxaca. Methods: We

constructed capture-recapture histories per species and roost, and for species for which we obtained recaptures

that represented at least 10 % of the captures, we used the probabilistic Cormack-Jolly-Seber model. In the case

of species with no recaptures or with a recapture proportion lower than 10 %, we estimated the number of indi-

viduals per roost by applying the same proportion between the number of captured specimens and the estimated

number for species with recaptures greater than 10 % and that they belonged to the same family or trophic guild.

Results: The total estimated number of bats in the three studied roosts was 20 105. The highest colony size esti-

mates were for the mormoopids Pteronotus fulvus and P. mesoamericanus from El Apanguito and P. fulvus from

Cerro Huatulco, with 6 609, 4 092 and 2 212 individuals, respectively. Conclusions: The methodology used in

this study allowed estimating the colony size for all registered species, even though only for 21.42 % the recap-

ture rates were greater than 10 %. Therefore, we consider that this methodology represents a viable alternative

to estimate colony size in other roosts. This information, together with the high species richness and importance

for reproductive processes, allow us to propose these sites as Bat Protection and Conservation Areas in Mexico.

Key words: abundance; capture-recapture; cave; chiropterans; Cormack-Jolly-Seber; mine.

Santos-Moreno, A., & Hernández-Aguilar, I. (2021). Estimation of bat colony size even

with low recapture rates: an example based on the Cormack-Jolly-Seber model in

Oaxaca, México. Revista de Biología Tropical, 69(1), 231-244. DOI 10.15517/rbt.

v69i1.38777

ISSN Printed: 0034-7744 ISSN digital: 2215-2075

Bat populations play a vital role in natural

ecosystems and have a significant positive

economic impact, particularly insectivore bat

populations in the control of agricultural pests

(Cleveland et al., 2006). Colony size is an

important variable to understand the biology

and ecology of organisms that live in groups.

It is also important for the implementation

of effective conservation actions for these

organisms and can also provide useful eco-

logical information, such as the amount of

dispersed seeds, dynamic of the community,

and foraging patterns (Hristov, Betke, Theri-

ault, Bagchi, & Kunz, 2010). However, esti-

mating colony size in the field is difficult and

has been both a logistical and technological

DOI 10.15517/rbt.v69i1.38777

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challenge, particularly for endangered, rare,

and cryptic species (Kunz & Anthony, 1996;

Kunz, 2003; McCracken, 2003; Kunz, Betke,

Hristov, & Vonhof, 2009). This is mainly due

to the biological characteristics of bats, such as

their small size, high vagility, and their strictly

nocturnal lifestyle, although it is also a result

of the methodologies employed. For example,

estimations of colony size using thermal imag-

ing are highly costly (Hristov, Betke, & Kunz,

2007) and visual counts and photographic esti-

mations can be prone to bias (O’Farrell & Gan-

non, 1999). Capture-mark-recapture (CMR)

methods, which consist in marking individuals

in a first capture session and then recording the

proportion of marked individuals in subsequent

recapture sessions, have been demonstrated to

be an efficient tool for the estimation of bat col-

ony size (Puechmaille & Petit, 2007). Although

to date there are no studies in which the popula-

tion size of ecologically similar and taxonomi-

cally related sympatric bat species is compared,

it is to be expected that when subjected to the

same environmental conditions they will show

similar population sizes, and therefore similar

probabilities of capture. The empirical data,

at least in the Mexican tropics, do not show a

clear pattern in this sense, since some studies

show a tendency for species of the same genus

to show similar abundances (e. g., Navarro &

Leon-Paniagua, 1995; Ramírez-Lucho, Coates,

& González-Christen, 2017), while in others

there is a clear predominance in the number of

captures of a species (e. g. Moreno & Halfter,

2001; Mendoza, Horváth, Ruiz, Escalona, &

Navarrete, 2017).

Given the low abundance of roosts that

contain colonies of thousands of bats world-

wide (Furey & Racey, 2016), it is necessary

to carry out estimations of colony size that

will help to obtain a better perspective of the

dynamics of bat populations across time. In

this sense, caves stand out due to their capacity

to maintain thousands or millions of individu-

als (Arita, 1993; Trajano & Giménez, 1998),

although they are also relatively more vulner-

able systems compared to other roosting sites

(Elliott, 2000; Hamilton-Smith & Eberhard,

2000) and are currently subject to threats (guano

mining, unsupervised tourist visits, vandalism,

and alteration and loss of surrounding vegeta-

tion cover) that put bat populations at risk and

could even lead to the extinction of species that

depend on cave roosts (Mickleburgh, Hutson,

& Racey, 2002; Medellín, 2003; Elliott, 2004;

Gunn, 2004; McCracken, 2011; Medellín, Wie-

derholt, & López-Hoffman, 2017).

Considering the above, there is an urgent

need to perform studies that provide infor-

mation about the identity and abundance of

species that occupy a given roosts, such as

caves and mine tunnels, in order to determine

which are the main populations and sites that

exhibit higher vulnerability and conservation

value (Kloepper et al., 2016). This is impor-

tant because in most conservation plans and

identification of areas in need of protection,

the parameters that are taken into account

are vegetation cover and forest fragmenta-

tion, while subterranean ecosystems (caves,

mines, cracks) tend to be underrepresented or

even ignored (Sugai, Ochoa-Quintero, Costa-

Pereira, & Roque, 2015; Medellín et al., 2017).

The roosts evaluated in this study had

not been previously explored, so there are no

previous studies that indicated the high diver-

sity of species that the three roosts harbor.

However, the results of the diversity (rich-

ness and abundance) of the three refuges have

been published recently (Hernández-Aguilar &

Santos-Moreno, 2020a), so work will continue

so that the three sites are considered impor-

tant sites for bat populations from Mexico.

Therefore, the objective of this study was to

estimate the colony size of 14 bat species that

were recorded throughout one year in a mine

and two caves. In addition, we present a new

method to estimate the colony size of species

with low recapture rates (< 10 %).

MATHERIALS AND METHODS

Study site: The study was carried out in a

mine tunnel (hereafter La Mina, 15º54’52’’ N &

96º24’59’’ W, and an altitude of 1 110 m.a.s.l),

in the municipality of Pluma Hidalgo, and two

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caves in Santa María Huatulco: El Apanguito

(15º51’58’’ N & 96º21’13.2’’ W, and an altitude

of 695 m.a.s.l) and Cerro Huatulco (15º50’59’’

N & 96º21’04.3’’ W, and an altitude of 475

m.a.s.l), located in the state of Oaxaca, Mexico

(Fig. 1). The entrances to La Mina are 3 m high

and 2 m wide, for El Apanguito it is 1.20 x 1.5

m and at Cerro Huatulco it is 10 x 15 m. The

Mine contains water for most of the year and

only Cerro Huatulco has four chambers, the

remaining two have only one chamber. A com-

plete description of the roosting sites can be

found in Hernández-Aguilar & Santos-Moreno

(2020a; 2020b). The climate is hot subhumid

with rainfall in the summer and the main veg-

etation in the zone is medium semi-evergreen

forest with coffee plantations (Trejo, 2004;

OEIDRUS, 2005).

Field work: We carried out monthly sam-

plings from June 2016 to June 2017, with a

duration of two nights per roost, including a

dry season (October-April) and a rainy season

(May-September). It was not possible to per-

form any sampling during the month of May

2017 due to adverse environmental conditions

that made it impossible to access La Mina.

Bats were captured with a G5 harp trap (Bat

Conservation and Management, Inc., Carlisle,

PA, EE. UU.), 1.5 m wide and 2 m high, that

was placed at the entrance of the roosts from

18:00 to 00:00. All captured individuals were

immediately placed in cloth bags and then

processed. We identified the species and deter-

mined the sex and age category (juvenile or

adult); according to the degree of the phalan-

geal epiphyses observed against the light of a

headlamp (Handley, Wilson, & Gardner, 1991).

Finally, we placed an aluminum ring (National

Band and Tag Company, Newport, Kentucky,

USA) on the forearm of each individual with a

unique serial identification number depending

on the size of the organism: category A (2.9

mm diameter) for species such as Pteronotus

Fig. 1. Geographic location of the three roosts evaluated in the municipalities

of Pluma Hidalgo and Santa María Huatulco, Oaxaca, Mexico.

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fulvus and Natalus mexicanus; and category B

(4 mm) for species such as Artibeus toltecus,

Carollia perspicillata, Glossophaga soricina,

Pteronotus mesoamericanus, and Mormoops

megalophylla. Once all the information was

recorded, we released the individuals in the

place where they were captured. In the case

of recaptured organisms, we obtained comple-

mentary data, such as time of recapture and

if the ring caused any damage to the forearm.

This study was carried out with a Scientific

Collection License for wildlife teaching grant-

ed by the Ministry of Environment and Natural

Resources (SEMARNAT-20/ks-0112/10/16).

Data analysis: We constructed capture-

recapture histories of individuals grouped by

species and roost. In the case of species with

recaptures that represented at least 10 % of

total captures, we applied a Cormack-Jolly-

Seber model was applied, which includes four

assumptions: 1) each animal marked in time (i)

has the same probability of being recaptured

); 2) each animal marked in the population

at time (i) has the same probability of surviving

time (i + 1); 3) the marks do not fall off or are

erased, they are detectable, and 4) the informa-

tion collection process is relative to the interval

of each time elapsed between time (i) and time

(i + 1). This model includes two parameters:

capture probability (p) and apparent survival

probability (ϕ). Each parameter can be constant

(p o ϕ) or vary across time (p

or ϕ

), which

results in four possible candidate models for

each species and roost. The final model for

each species and roost was selected based on

the Akaike Information Criterion for small

samples (AICc, Burnham & Anderson, 2002).

Estimations were performed in Mark version

8.2 (White & Burnham, 1999). Once the final

model was selected, we estimated the value

or values of p (when the final model included

this parameter as constant or varying across

time, respectively) and used them to estimate

monthly population sizes (N) as the ratio of

the number of captured individuals (n) and the

capture probability (p): N= n/p (Lindenmayer,

Lacy, & Viggers, 1998). In order to apply the

Cormack-Jolly-Seber model to species with no

recaptures or a recapture proportion lower than

10 % of the captures, we estimated the number

of individuals per roost by applying the same

proportion between the number of captured

specimens and the estimated number for the

recorded species that belonged to the same

family or to the same trophic guild. For the

phyllostomid bat species Artibeus jamaicensis,

A. toltecus, A. watsoni, Desmodus rotundus,

Glossophaga soricina, Sturnira hondurensis,

and Carollia perspicillata from El Apanguito

and Cerro Huatulco, the estimated number

was obtained by applying the same proportion

between the number of captured specimens and

the estimated number for Carollia perspicil-

lata from La Mina, whose capture probability

had a narrower confidence interval than that

of A. toltecus in the same roost. In the case of

the mormoopid species Pteronotus fulvus, P.

mesoamericanus, and P. psilotis, values were

calculated with the proportion observed for

insectivorous bat Mormoops megalophylla in

El Apanguito, which was the only species of

this family for which we obtained enough data

to estimate capture probabilities. Moreover,

this species shares ecological similarities with

other species of the same family and can form

large colonies, as those observed in the genus

Pteronotus. Given that we did not record

M. megalophylla in El Apanguito during the

months of May, June, and July and could not

estimate the proportion between the number of

captured individuals and the number estimated

with the Cormack-Jolly-Seber model, we con-

sidered the mean value of the proportions of the

months when the species was recorded (from

September to April). In the case of Balantiop-

terix plicata (Emballonuridae), Natalus mexi-

canus (Natalidae), and Myotis pilosatibialis

(Vespertilionidae), which did not have recap-

ture proportions higher than 10 % in any roost

or an ecologically similar species, proportions

were calculated in the same way as for mor-

moopids, which did not have recaptures or had

recaptures lower than 10 % of total captures.

The number of individuals per roost and month

was calculated as the sum of the estimates of

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each species present, while the total per roost

was calculated conservatively as the sum of the

maximum estimated number monthly of each

species for each roost throughout the year. This

restriction was applied because we do not know

the number of individuals that remain in each

refuge throughout the year and many individu-

als would be re-counted as much as 12 times

if we the sum of all the monthly estimates of

each species.

RESULTS

We captured, marked, and released 5 788

bats of 14 species, 10 genera, and five families:

one emballonurid (Balantiopterix plicata), one

natalid (Natalus mexicanus), four mormoopids

(Mormoops megalophylla, Pteronotus fulvus, P.

mesoamericanus, and P. psilotis), seven phyl-

lostomids (Artibeus jamaicensis, A. toltecus,

A. watsoni, Carollia perspicillata, Desmodus

rotundus, Glossophaga soricina, and Sturnira

hondurensis), and one vespertilionid (Myotis

pilosatibialis). The most abundant species were

P. fulvus and P. mesoamericanus with 41.01

and 32.34 % of the captures, respectively, and

the least abundant species were G. soricina

(3.11 %) and A. toltecus (1.31 %). We captured

570 individuals in La Mina, 4 306 in El Apan-

guito and 960 in Cerro Huatulco (Table 1).

The Cormack-Jolly-Seber model was

applied only to the data of A. toltecus (16.92

% recaptures) and Carollia perspicillata

(15.79 %), both in La Mina, and Mormoops

TABLE 1

Number of captured (first number) and estimated (second number) bats per month per roost for species or colonies to

which we could not apply capture-recapture models (recapture proportions lower than 10 %)

Month

Max

Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun

Roost

Balantiopterix plicata

La Mina 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0

CCH 1-13 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 1-13

CEA 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0

Total 1-13 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0

Natalus mexicanus

La Mina 1-13 1-13 0-0 1-13 0-0 0-0 1-13 0-0 0-0 0-0 0-0 0-0 1-13

CCH 0-0 0-0 0-0 1-13 0-0 0-0 0-0 1-13 3-40 0-0 0-0 0-0 3-40

CEA 0-0 12-159 28-371 17-225 61-808 17-225 18-238 11-146 15-199 13-172 3-40 4-53 61-808

Total 1-13 13-172 28-371 19-251 61-808 17-225 19-251 12-159 18-239 13-172 3-40 4-53

Mormoops megalophylla

La Mina 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0

CCH 6-79 0-0 2-27 0-0 1-13 0-0 1-13 0-0 0-0 0-0 6-79 13-172 13-172

Total 6-79 0-0 2-27 0-0 1-13 0-0 1-13 0-0 0-0 0-0 6-79 13-172

Pteronotus fulvus

La Mina 0-0 0-0 0-0 0-0 0-0 0-0 1-13 0-0 1-13 0-0 0-0 0-0 1-13

CCH 6-79 81-1 070 70-928 37-490 167-2 212 78-1 033 23-305 110-1 457 100-1 325 68-901 8-106 10-132 167-2 212

CEA 0-0 2-26 151-2 001 65-861 138-1 828 190-2 516 177-2 345 499-6 609 311-4 119 38-504 27-358 11-146 499-6 609

Total 6-79 83-1 096 221-2 929 102-1 351 305-4 040 268-3 549 201-2 663 609-8 066 412-5 457 106-1 405 35-464 21-278

Pteronotus mesoamericanus

La Mina 2-26 10-132 41-543 14-185 16-212 8-106 15-199 1-13 0-0 5-66 0-0 0-0 41-543

CCH 12-159 6-79 9-119 12-159 1-13 1-13 0-0 3-40 4-53 1-13 17-225 8-106 17-225

CEA 58-768 108-1 427 136-1 802 216-2 860 117-1 550 88-1 165 74-980 114-1 510 74-980 186-2 466 202-2 675 309-4 092 309-4 092

Total 72-953 124-1 638 186-2 464 242-3 204 134-1 775 97-1 284 89-1 179 118-1 563 78-1 033 192-2 545 219-2 900 317-4 198

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TABLE 1 (Continued)

Month

Max

Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun

Pteronotus psilotis

La Mina 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0

CCH 2-26 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 2-26

CEA 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0

Total 2-26 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0

Desmodus rotundus

La Mina 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0

CCH 17-363 0-0 0-0 0-0 2.42 0-0 0-0 0-0 0-0 0-0 2.42 0-0 17-363

CEA 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0

Total 17-363 0-0 0-0 0-0 2.42 0-0 0-0 0-0 0-0 0-0 2.42 0-0

Glossophaga soricina

La Mina 0-0 0-0 11-235 10-214 27-576 6-128 7-149 11-234 19-406 39-833 0-0 0-0 39-833

CCH 2-43 4-85 0-0 2-42 33-704 0-0 0-0 0-0 0-0 0-0 11-235 0-0 33-704

CEA 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0

Total 2-43 4-85 11-235 12-256 60-1 280 6-128 7-149 11-234 19-406 39-833 11-235 0-0

Carollia perspicillata

CCH 0-0 1-21 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 1-21

CEA 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0

Total 0-0 1-21 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0

Artibeus jamaicensis

La Mina 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0

CCH 12-256 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 3-64 2-42 12-256

CEA 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0

Total 12-256 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 3-64 2-42

Artibeus toltecus

CCH 1-21 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 1-21

CEA 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0

Total 1-21 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0

Artibeus watsoni

La Mina 0-0 2-43 0-0 0-0 3-64 0-0 0-0 1-21 1-21 0-0 0-0 0-0 3-64

CCH 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0

CEA 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0

Total 0-0 2-43 0-0 0-0 3-64 0-0 0-0 1-21 1-21 0-0 0-0 0-0

Sturnira hondurensis

La Mina 2-43 1-21 2-43 0-0 1-21 0-0 0-0 0-0 0-0 0-0 0-0 1-21 2-43

CCH 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 1-21 0-0 1-21

CEA 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0

Total 2-43 1-21 2-43 0-0 1-21 0-0 0-0 0-0 0-0 0-0 1-21 1-21

Myotis pilosatibialis

La Mina 0-0 0-0 0-0 1-13 3-40 0-0 0-0 0-0 1-13 0-0 0 -0 1-13 3-40

CCH 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0

CEA 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0 0-0

Total 0-0 0-0 0-0 1-13 3-40 0-0 0-0 0-0 1-13 0-0 0-0 1-13

Max=Maximum number of bats per roost per species throughout the entire sampling year. CCH: Cave Cerro Huatulco;

CEA: Cave El Apanguito.

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megalophylla in El Apanguito (13.17 %). For

C. perspicillata and A. toltecus in La Mina,

the final model was the one where both cap-

ture probability and apparent survival were

constant throughout the year (ϕp), whereas

for Mormoops megalophylla in El Apanguito,

apparent survival was also constant across the

whole sampling period, but capture probabili-

ties varied monthly (ϕp

; Table 2). For the three

species, the best supported models presented

weights of 95.37, 99.21, and 98.77, respec-

tively. The capture probabilities estimated for

C. perspicillata and A. toltecus in La Mina and

M. megalophylla in El Apanguito were very

low, lower than 0.1. For C. perspicillata in La

Mina, we estimated a population size of 684

individuals throughout the year, with monthly

fluctuations between 107 (March) and 684

(September). For A. toltecus, we estimated 183

individuals, with a maximum abundance in

July (183 individuals) and a minimum abun-

dance in December and January (23 individu-

als in each month). For M. megalophylla in El

Apanguito, we estimated a total population size

of 2 106 individuals, with a maximum in March

(2 106 individuals) and a minimum in June and

July (0) (Table 3).

Even though we obtained recaptures of

four other species from the three roosts (Glos-

sophaga soricina in La Mina with 2.36 % of

recaptures, Pteronotus mesoamericanus in La

Mina and El Apanguito with 3.77 and 4.55 %,

respectively, P. fulvus in Cerro Huatulco with

0.39 % and in El Apanguito with 3.67 %, and

TABLE 2

Comparison of four candidate models and parameters of the final model (standard error of the estimation in parenthesis)

for the three bat species that had recapture proportions higher than 10 %

Candidate

Model

AICc ∆AICc

AICc

Weights

Model

Likelihood

Num.

Par.

Deviance

Final model

Parameter= Value (EE)

Carollia perspicillata La Mina

ϕp 222.7785 0 0.9537 1 2 80.4352 ϕ=0.8585 (0.9500)

ϕp

228.8673 6.0888 0.0454 0.0476 11 66.9147 p=0.0467 (0.0899)

p 236.7892 14.0107 0.0008 0.0009 11 74.8366

244.5441 21.7656 0.00002 0 19 63.1724

Artibeus toltecus La Mina

ϕp 97.0229 0 0.9921 1 2 42.6725 ϕ=0.7286 (0.8815)

ϕp

111.5070 14.4841 0.0007 0.0007 11 34.8584 p=0.0876 (0.2042)

p 116.0200 18.9971 0.00007 0.0001 11 39.3715

127.5036 30.4807 0 0 19 24.4276

Mormoops megalophylla El Apanguito

ϕp

763.4193 0 0.9877 1 9 46.9828 ϕ=0.7818 (0.8784)

772.9295 9.5102 0.0085 0.0086 15 44.099 p

September

= 0 (0)

p 774.5513 11.1320 0.0037 0.0038 9 58.1148 p

October

=0 (0)

ϕp 785.3180 21.8987 0.00002 0 2 83.0995 p

November

=0.0299 (0.1134)

December

=0.0679 (0.1230)

January

=0.1181 (0.1877)

February

=0.1218 (0.1932)

March

=0.0807 (0.1367)

April

=0.0212 (0.0487)

AICc = Akaike Information Criterion for small samples. ∆AICc = difference in AICc between the respective model and

the best candidate model. Num. Par. = Number of parameters. p = capture probability. Φ = apparent survival probability.

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Natalus mexicanus in El Apanguito with 1.52

% recaptures), the proportions with respect to

the number of captures were lower than 10 %,

and we were not able to apply the Cormack-

Jolly-Seber model. There were no recaptures

for the rest of the species, but we were able

to obtain an estimation of colony size using

the methodology described above. We did not

observe any species that was consistently the

most abundant in the three roosts. In El Apan-

guito, we obtained the highest estimations for

P. fulvus in February (6 609 individuals), for

P. mesoamericanus in June (4 092), and for

N. mexicanus in November (808). In La Mina,

the highest estimated number of individuals

for G. soricina was observed in April (833

individuals), for A. watsoni in November (64

individuals), for S. hondurensis in July and

September (43 individuals), and for M. pilo-

satibialis in November (40 individuals), while

in Cerro Huatulco, the highest estimations for

D. rotundus, A. jamaicensis, P. psilotis, and B.

plicata were obtained in July with 363, 256, 26,

and 13 individuals, respectively (Table 1).

In the complex comprised of the three stud-

ied roosts, we estimated the presence of 20 105

bats, with 67.71 % in El Apanguito, 12.01 %

in La Mina, and 20.26 % in Cerro Huatulco.

Overall, we estimated a monthly mean value

of 525.15 bats in La Mina, with a maximum

in September (1 318) and a minimum in May

(0). In Cerro Huatulco, the monthly mean was

of 339.5 individuals, with a maximum (2 916)

in November and a minimum (0) in September

and October, December to February and April.

In El Apanguito, the monthly mean was of

1 309 individuals, with a maximum (4 092) in

June and a minimum (0) in July and May.

DISCUSSION

We obtained recapture rates higher than 10

% only for three bat species (C. perspicillata

15.79 %, A. toltecus 16.92 %, and M. megalo-

phylla 13.17 %), and lower than 10 % for four

species (G. soricina 2.36 %, P. mesoamerica-

nus 5.51 %, P. fulvus 3.95 %, and 1.52 % for N.

mexicanus); we did not record any recaptures

for the other seven species. In the latter two

cases, it was not possible to apply the Cor-

mack-Jolly-Seber model or, if it was applied,

the resulting estimations are not accurate. Thus,

TABLE 3

Monthly number of captured (first number) and estimated bats with the probabilistic Cormack-Jolly-Seber model

(second number) in three roosts for the three species that had recapture proportions higher than 10 %

Month

Carollia perspicillata Artibeus toltecus Mormoops megalophylla

La Mina La Mina El Apanguito

July 23 - 491 16 - 183 0 - 0

August 17 - 363 4 - 46 14 - 185

September 32 - 684 8 - 91 12 - 159

October 10 - 214 3 - 34 66 - 874

November 25 - 534 14 - 160 143 -1 894

December 8 - 171 2 - 23 99 - 1 311

January 10 - 214 2 - 23 133 - 1 762

February 20 - 427 3 - 34 155 - 2 053

March 5 - 107 15 - 171 159 - 2 106

April 19 - 406 4 - 46 35 - 464

May 0 - 0 0 - 0 0 - 0

June 7 - 150 5 - 57 0 - 0

Mean 15 - 313 6 - 72 68 - 901

Min 0 - 0 0 - 0 0 - 0

Max 32 - 684 16 - 183 159 - 2 106

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the implementation of new methodologies is

necessary to obtain estimations with extremely

low recapture rates as occur with large colonies

of bats. In our study, the two most abundant

species (P. fulvus with 2 369 individuals and

P. mesoamericanus with 1 868 individuals)

had such low recapture rates (3.95 % and 5.51

%, respectively, perhaps because they occupy

other alternative refuges, since we have identi-

fied three caves near El Apanguito and Cerro

Huatulco) that it was not possible to directly

apply the model. However, with the methodol-

ogy implemented in this study and taking the

proportion between the number of captures and

the estimated colony size of M. megalophylla,

it was possible to estimate the colony size of

the mormoopids P. fulvus and P. mesoamerica-

nus, obtaining thus the largest colony sizes in

El Apanguito with 6 609 and 4 092 individuals,

respectively.

The specific ecological characteristics of

each species, such as roost fidelity, use of

alternative roosts, flight patterns, the echoloca-

tion abilities to detect the net, and large colony

sizes make it difficult to obtain high recapture

rates, which makes it difficult to estimate their

colony sizes (Lewis, 1995; Storz, Balasingh,

Nathan, Emmanuel, & Kunz, 2000; Godoy

et al., 2002; Chaverri & Kunz, 2006). The

overall recapture percentage (average 6.1 %)

were similar to those reported in other studies

in México, North America (United States 40

%, Stevenson & Tuttle, 1981; Canada 14 %,

Norquay, Martinez-Núñez, Dubois, Monson, &

Willis, 2013), and South America (Brazil 0 %,

Zortéa, Bastos, & Acioli, 2015; 1 %, McCrak-

en, 2003; 27.4%, Trajano, 1996). In this sense,

for bat species with recaptures lower than 10 %,

we consider it appropriate to use the approach

applied in the present study, where colony size

was estimated by using the proportions of the

observed number and the number estimated for

species with recapture percentages higher than

10 % that are ecologically similar and share

the same roost. Although this method has not

been applied before in bat species, it is to be

expected that when subjected to the same envi-

ronmental conditions they will show similar

population sizes and, therefore, similar capture

probabilities. Although it should be noted that

the precision of this method should be proven

in subsequent studies.

The estimations of colony size obtained

with the Cormack-Jolly-Seber capture-recap-

ture model are reasonable for the three studied

species (M. megalophylla with 2 106 indi-

viduals throughout the year in El Apanguito

and C. perspicillata with 684 individuals and

A. toltecus with 183 individuals in La Mina)

if we consider that the estimated values are

within the range known of colony size for

these species. For example, M. megalophylla is

cave-specialist species that can form colonies

from less than 1 000 individuals (Torres-Flores,

López-Wilchis, & Soto-Castruita, 2012) to up

to 500 000 individuals (Bonaccorso, Arends,

Genoud, Canton, & Morton, 1992; Iñiguez-

Dávalos, 2005). In the cave system Cuevas del

Silvino in Guatemala, the colony size of this

species was estimated to be of approximately

44 200 individuals using video cameras (Cajas-

Castillo, Echeverría, & Trujillo, 2015). In the

case of C. perspicillata and A. toltecus, low

population sizes have been reported through-

out their distribution area in Mexico (Jalisco,

Iñiguez-Dávalos, 1993; Stoner, 2002; Queré-

taro, Navarro & León-Paniagua, 1995; Oaxa-

ca, García-García, & Santos-Moreno, 2008),

which could be related to specific requirements

of the roosts such as temperature, humidity, air

flow, or light intensity, the diversity of other

available roosts, and the availability of food,

which could limit the presence of large popu-

lations (over 1 000 individuals according to

Arita, 1993). Artibeus toltecus, together with A.

watsoni and S. hondurensis, apart from roost-

ing in caves, also form small colonies in tents

constructed with leaves, holes in trees, tunnels,

cracks in rocks, and abandoned constructions

(Kunz & McCracken, 1996; McCracken &

Wilkinson, 2000; Chaverri & Kunz, 2006).

Other species with large colony sizes were P.

mesoamericanus and P. fulvus, with colony

size estimations of over 20 000 individuals

throughout the year in El Apanguito. These are

cave-specialist species that can form colonies

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of thousands of individuals (Bonaccorso et al.,

1992; Arita, 1993; Ortega, 2005). Other stud-

ies that have carried out estimations for these

species, through direct observations in Mexico

(Torres-Flores et al., 2012) and video cameras

in Guatemala (Cajas-Castillo et al., 2015), have

reported colonies of over 6 000 individuals for

P. mesoamericanus and up to 98 600 individu-

als for P. fulvus (Cajas-Castillo et al., 2015).

In the case of N. mexicanus, we captured 199

individuals and estimated a colony size of 2

636 individuals in El Apanguito, 66 in Cerro

Huatulco, and 52 in La Mina. This species has

been observed to form colonies of up to 5 000

individuals, but it is generally found in colo-

nies between 100 and 200 individuals (Torres-

Flores & López-Wilchis, 2010). Finally, the

estimated colony size of G. soricina was of

833 individuals in La Mina and 704 individuals

in Cerro Huatulco. For this species, estimated

colony sizes have been of less than 500 indi-

viduals in other caves in Mexico (Torres-Flores

et al., 2012). Therefore, the estimates obtained

in this study are higher than those estimated in

other areas, so the precision and usefulness of

this method should be tested in the future. We

found considerable variation in the monthly

estimations of the species recorded in all three

roosts, which suggests that the composition of

the colonies exhibits considerable dynamics

(Hristov et al., 2010).

The total estimated number of bats in the

three studied roosts was 20 105, with higher

concentrations in El Apanguito (13 615 indi-

viduals) and Cerro Huatulco (4 074 individu-

als). These estimations, together with high

species richness, reproduction processes, and

occupation dynamics between these roosts

(Hernández-Aguilar & Santos-Moreno, 2020a;

Hernández-Aguilar & Santos-Moreno, 2020b),

allow us to propose these sites as Bat Protec-

tion and Conservation Areas in Mexico. We

also recommend continuing to monitor the

bat populations of these sites and, if possible,

implementing other methods to evaluate the

accuracy of our estimations.

Some studies have demonstrated that the

use of video cameras to record bats emerging

from roosts (Escalona-Segura, Vargas-Contre-

ras, & Sosa, 2002; Vargas-Contreras, Escalo-

na-Segura, Arroyo, Rendon Von Osten, &

Navarro, 2012; Cajas-Castillo et al., 2015)

and the incorporation of acoustic recordings

(Kloepper et al., 2016) could be techniques

that may produce robust estimations of size of

bat colonies. Thus, further studies using these

techniques could complement our results or

even improve estimates of the number of bats

that use the roosts, as well as provide the tools

that allow to establish priority criteria for the

conservation of roosts and bats in the area.

Even though recent advances, such as digi-

tal photography and image analysis, in some

cases allow estimating the number of individu-

als emerging from a roost (Corso, Woolley, &

Lacher, 2010), they do not allow to determine

the species identity and, thus, it is not pos-

sible to know the colony size of each species,

except in cases where the roost includes only

one species. This is the same limitation of pas-

sive acoustic methods (Kloepper et al., 2016),

thermal detection systems (Otálora-Ardila et

al., 2020), and thermal infrared imaging and

computer vision analysis (Hristov et al., 2010).

The Light Detection and Ranging (LiDAR)

scanning system allows to estimate the num-

ber of individuals per species by scanning the

roosts and visually recognizing and labelling

the areas occupied by each species (Shazali

et al., 2017); however, the cost of this system

is currently too high for its generalized use.

Very recently, genetic tag-recapture methods

are expensive but seem to offer advantages

over other more invasive methods, although

it is only recommended for species that show

high fidelity to the refuge and that do not form

colonies of thousands or millions of individu-

als (Oyler-McCance et al., 2018). Therefore,

we consider that the estimation method used

in the present study provides a low-cost, and

reasonably reliable option for the estimation of

bat colony size, especially for roosts occupied

by more than one species.

Ethical statement: authors declare that

they all agree with this publication and made

241

Rev. Biol. Trop. (Int. J. Trop. Biol.) • Vol. 69(1): 231-244, March 2021

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 acknowledge-

ments section. A signed document has been

filed in the journal archives.

ACKNOWLEDGMENTS

We thank the municipal authorities of

Pluma Hidalgo and Santa María Huatulco for

providing the facilities and permits to carry

out this study. To all the people that helped

with the field work and the ringing of bats. To

A.G. Ramos-Fernández, M.U. García Guer-

rero, M. Rös, and J. Williams for reviews prior

to the preparation of the manuscript. To M.

Calixto-Rojas for preparing the study map. To

the Instituto Politécnico Nacional de México

for providing financial support to carry out

this project (projects SIP-20161645 and SIP-

20171154 to the first author). The Consejo

Nacional de Ciencia y Tecnología de México

provided a scholarship for postgraduate studies

to the second author.

RESUMEN

Estimación del tamaño de colonia en murciéla-

gos incluso con bajas tasas de recaptura: un ejemplo

basado en el modelo Cormack-Jolly-Seber en Oaxaca,

México. Introducción: El tamaño del grupo o colonia

es una variable importante que está relacionada con los

aspectos biológicos, ecológicos y de conservación de los

murciélagos. Sin embargo, estimar el tamaño de cada colo-

nia o grupo en refugios utilizados por más de una especie

es particularmente difícil, especialmente cuando las tasas

de recaptura son muy bajas (< 10 %). Objetivo: Estimar

el tamaño de la colonia de 14 especies de murciélagos: un

emballonúrido, un natálido, cuatro mormópidos, siete filos-

tómidos y un vespertiliónido, que se refugiaron durante un

año (Julio 2016 a Junio 2017) en una mina y dos cuevas

-Cerro Huatulco y El Apanguito- en la Sierra Sur y Costa

del estado de Oaxaca. Métodos: Construimos historias de

captura-recaptura por especie y refugio, y para las especies

que se obtuvieron recapturas que representaban al menos

el 10 % de las capturas, utilizamos un modelo probabi-

lístico de Cormack-Jolly-Seber para estimar el tamaño de

sus colonias. En el caso de especies sin recapturas o con

una proporción de recaptura inferior al 10 %, estimamos

el número de individuos por refugio aplicando la misma

proporción entre el número de individuos capturados y

el número total estimado para las especies con recapturas

mayores del 10 % y que pertenecieran a la misma familia

o gremio trófico registradas con la mayor similitud eco-

lógica y con suficientes recapturas para aplicar el modelo

Cormack-Jolly-Seber. Resultados: El número total esti-

mado de murciélagos en los tres refugios de estudio fue de

20 105. Las estimaciones de tamaño de colonia más altos

fueron para los mormópidos Pteronotus fulvus y P. mesoa-

mericanus de El Apanguito y P. fulvus en Cerro Huatulco,

con 6 609, 4 092 and 2 212 individuos, respectivamente.

Conclusiones: La metodología utilizada en este estudio

permitió estimar el tamaño de la colonia para todas las

especies registradas, a pesar de que solo para el 21.42 %

las tasas de recaptura fueron superiores al 10 %. Por lo

tanto, consideramos que esta metodología representa una

alternativa viable para estimar el tamaño de colonia en

otros refugios. Esta información, junto con los procesos de

alta riqueza de especies y reproducción que tienen lugar

en esta área, permiten proponer estos sitios como áreas de

protección y conservación de murciélagos en México.

Palabras clave: abundancia; captura-recaptura; Cormack-

Jolly-Seber; cueva; mina; quirópteros.

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