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1072
Seasonal ecology of a migratory nectar-feeding bat at the edge of
its range
Winifred f. frick,* Paul a. Heady iii, alexis d. earl, Maria clara arteaga, Patricia cortés-calva, and
rodrigo a. Medellín
Bat Conservation International, Austin, TX 78746, USA (WFF)
Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, CA 95060, USA (WFF)
Bat Conservation Research and Services, Aptos, CA 95001, USA (PAH)
Conservation Metrics, Inc., Santa Cruz, CA 95060, USA (ADE)
Departamento de Biología de la Conservación, Centro de Investigación Científica y de Educación Superior de Ensenada
(CICESE), Carretera Ensenada-Tijuana N. 3918, Zona Playitas, C.P. 22860 Ensenada, Baja California, México (MCA)
Programa de Planeación Ambiental, Centro de Investigaciones Biológicas del Noroeste, Av. Instituto Politécnico Nacional 195,
C.P. 23096 La Paz, Baja California Sur, México (PC-C)
Departamento de Ecología de la Biodiversidad, Instituto de Ecología, Universidad Nacional Autónoma de México, Apartado
Postal 70-275, México Distrito Federal 04510, México (RAM)
* Correspondent: wfrick@batcon.org
Migratory species that cross geopolitical boundaries pose challenges for conservation planning because threats
may vary across a species’ range and multi-country collaboration is required to implement conservation action
plans. The lesser long-nosed bat (Leptonycteris yerbabuenae) is a migratory pollinator bat that was removed
from the Endangered Species List in the United States in 2018 and from threatened status in Mexico in 2013.
The seasonal ecology and conservation status of the species is well understood in the core part of its range on
mainland Mexico and in the southwestern United States, but relatively little is known about the species on the
Baja California peninsula in northwestern Mexico, a part of its range range separated by the Gulf of California.
We studied the seasonal ecology of lesser long-nosed bats on the Baja peninsula at 8 focal roosts along a 450-
km north-to-south transect to test hypotheses about migratory or residential status of the species on the Baja
peninsula. We provide evidence of an extensive population of lesser long-nosed bats on the Baja peninsula that
is primarily seasonally migratory and includes 2 mating roosts with males on the southern part of the peninsula.
Seasonal ecology of lesser long-nosed bats was closely associated with the flowering and fruiting season of the
cardón (Pachycereus pringlei), the dominant columnar cactus on the peninsula. However, we discovered that
some female lesser long-nosed bats arrive and give birth at southern roosts in mid-February, about 2 months
earlier than other migratory populations in more northern Sonoran Desert habitats. We documented the loss of
nearly a third of the known maternity roosts during the study, demonstrating that action to protect key roosts
remains a high priority. Migratory pollinators are particularly vulnerable to climate and land-use changes and we
recommend continued monitoring and research to guide effective range-wide conservation of the species.
Las especies migratorias o con rangos de distribución amplios que incluyen fronteras geopolíticas, representan
desafíos particulares para la planificación de estrategias de conservación, ya que las amenazas así como las
tendencias poblacionales pueden variar a lo largo de su rango geográfico y se requiere la colaboración de
múltiples países para implementar planes de acción que permitan su conservación. El murciélago magueyero
menor (Leptonycteris yerbabuenae) es un murciélago polinizador migratorio que recientemente fue sacado de
la lista de especies en peligro en los Estados Unidos en 2018 y en México en 2013. La ecología estacional
y el estatus de conservación de esta especie, ha sido bien estudiado en el centro de su rango de distribución
en México continental, pero se sabe muy poco acerca de la especie en la Península de Baja California en el
noreste de México, región que está separada del resto del rango por el golfo de California. Nosotros estudiamos
Journal of Mammalogy, 99(5):1072–1081, 2018
DOI:10.1093/jmammal/gyy088
Published online July 27, 2018
© The Author(s) 2018. Published by Oxford University Press on behalf of American Society of Mammalogists.
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://
creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the
original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
FRICK ET AL.—SEASONAL ECOLOGY OF A MIGRATORY BAT 1073
la ecología estacional del murciélago magueyero menor, en ocho cuevas a lo largo de un transecto de 450 km
norte-sur, en la Península de Baja California y pusimos a prueba la hipótesis del status migratorio o residente de
sus poblaciones en esta región. Proporcionamos la primera evidencia de una extensa población de esta especie
en la península, a cual es principalmente migratoria estacional e incluye dos cuevas de reproducción ubicadas
al sur de esta región. La ecología estacional del murciélago magueyero menor estuvo fuertemente asociada con
la estación de floración y fructificación del cardón (Pachycereus pringlei), el cactus columnar dominante en la
península. Nosotros también descubrimos que algunas hembras llegan y dan a luz en las cuevas más sureñas, a
mediados de febrero, cerca de dos meses antes que otras poblaciones migratorias, en el desierto de Sonora del
norte. Durante el tiempo de este estudio, documentamos la destrucción de una de las cuevas de maternidad, lo que
demuestra la necesidad de acciones de conservación para proteger estos refugios. Los polinizadores migratorios
son particularmente vulnerables a cambios en el uso del suelo y al cambio climático y recomendamos continuar
con el monitoreo y la investigación, con el fin de guiar su conservación a lo largo de todo el rango de distribución
de la especie.
Key words: Baja California Sur, cactus, conservation, Leptonycteris yerbabuenae, Mexico, migration, pollinator, range edge
Migratory or wide-ranging species that cross geopolitical
boundaries pose particular challenges for conservation plan-
ning as threats and population trends may vary across a spe-
cies’ range, and multi-country collaboration is required for
implementing conservation action plans (Medellín et al. 2004).
Conservation attention often focuses on core populations where
data may be more easily obtainable, but threats to and resiliency
of populations may differ across a species’ range (Channell and
Lomolino 2000). Understanding ecological differences across
a species’ range is important for predicting range shifts and
the impacts of climate change on patterns of global biodiver-
sity, particularly for areas where land use and climate change
are predicted to significantly alter habitat suitability (Zamora-
Gutierrez et al. 2018). Studying ecological dynamics at range
edges answers basic questions about biogeographic limits, but
is also needed to assess global extinction risk and inform con-
servation priorities at a species level (Channell and Lomolino
2000).
The lesser long-nosed bat (Leptonycteris yerbabuenae) is a
migratory nectar- and fruit-feeding bat that forms large aggre-
gations (up to hundreds of thousands of bats) in caves and
mines and migrates from central Mexico to the southwestern
United States during the spring and summer bloom of agave
and columnar cacti (Wilkinson and Fleming 1996; Ceballos
et al. 1997; Horner et al. 1998; Rojas-Martínez et al. 1999;
Stoner et al. 2003). The species was federally protected as
endangered in the United States at the northern extent of its
seasonal migratory range in the late 1980s (Cole and Wilson
2006), and recently became the first bat to be removed from
the Endangered Species List in the United States (USFWS
2018). The species was also listed in Mexico as threatened in
1994, and delisted in 2013 (Medellín et al. 2018). Population
dynamics, migratory patterns, and reproductive phenology are
relatively well-known in mainland Mexico (Wilkinson and
Fleming 1996; Ceballos et al. 1997; Horner et al. 1998; Rojas-
Martínez et al. 1999; Stoner et al. 2003) and monitoring of key
roosts in this central part of the range supported the delisting of
the species in Mexico (Medellín et al. 2018).
In contrast, the population status, seasonal ecology, and
migratory habits of lesser long-nosed bats on the Baja
California peninsula, a part of the species’ range separated by
the Gulf of California (Fig. 1), have received little attention.
Habitats on the Baja California peninsula are identified as at
high risk for loss of environmental suitability for bats over the
next 30 years due to land use and climate change (Zamora-
Gutierrez et al. 2018). In the USFWS species recovery plan,
only 2 roost sites for lesser long-nosed bats were listed on the
Baja California peninsula (USFWS 1995) and the assumption
Fig. 1.—Map of locations of 8 lesser long-nosed bat (Leptonycteris
yerbabuenae) roosts studied on the Baja California peninsula in north-
western Mexico. The Mulegé and Carmen roosts occur in the mid-
peninsular region and the other roosts are located in the southern Cape
region of the Baja peninsula.
1074 JOURNAL OF MAMMALOGY
was made that the Baja population was limited to year-round
residents that overwinter in the southern part of the peninsula
(Fleming et al. 1993; Rojas-Martínez et al. 1999). Earlier work
has shown that lesser long-nosed bats are widespread during
April and May on the Baja peninsula and associated islands in
the Gulf of California (Frick et al. 2007, 2009) and are regular
visitors to flowers of the cardón cactus (Pachycereus pringlei,
Cactaceae—Frick et al. 2013). Assessing the seasonal phenol-
ogy and population status of lesser long-nosed bats on the Baja
peninsula provides an opportunity to study how seasonal ecol-
ogy may differ at the northwestern edge of the range and fills
existing data gaps for assessing range-wide threats and popula-
tion status to determine species-level conservation needs of this
binational migratory species.
The migratory or resident status of lesser long-nosed bats on
the Baja peninsula has long been speculated about in the litera-
ture (Woloszyn and Woloszyn 1982; Fleming et al. 1993; Rojas-
Martínez et al. 1999). Two alternative hypotheses of migratory
behavior on the Baja peninsula have been proposed: 1) Female
bats seasonally migrate over the Gulf of California (potentially
using islands as “stepping stones”—Ramirez 2011), returning
to maternity roosts on the Baja peninsula to give birth and raise
young when columnar cacti and agave are in bloom in April
and May. This pattern would be consistent with the seasonal
phenology of populations that migrate to the Sonoran Desert
in northern mainland Mexico and the southwestern United
States where females arrive and give birth synchronously with
the bloom of columnar cacti and agaves (Rojas-Martínez et al.
1999). 2) Females reside year-round on the Baja peninsula and
spend the winter months in the southern Cape region of Baja
(south of La Paz) where they depend on winter-blooming aga-
ves (Fleming et al. 1993). If the latter hypothesis were true, we
would expect to find year-round occupancy and increased col-
ony sizes at southern roosts during winter months when bats are
absent from maternity sites in mid-peninsular areas.
We measured seasonal roost occupancy, reproductive timing,
and changes in body mass of lesser long-nosed bats on the Baja
peninsula to assess the seasonal ecology of the species on the
edge of its range. We compared seasonal occupancy patterns
and reproductive timing at roosts in the southern Cape region
of Baja to roosts in the mid-peninsular region to distinguish
between the 2 competing hypotheses of seasonal presence on
the Baja peninsula. We hypothesized that body mass of bats on
the Baja peninsula would vary seasonally and be highest during
spring and summer months when nectar and fruit from colum-
nar cacti, the dominant food resource, are abundantly available.
We also assess the conservation status of known roosts in Baja
and discuss the conservation implications of our findings.
Materials and Methods
Study area.—We studied the seasonal ecology of lesser long-
nosed bats in Sonoran Desert habitats of the Baja California
peninsula in northwestern Mexico (Fig. 1). The Baja California
peninsula has distinct ecoregions (http://bajaflora.org/) with
characteristic dominant plant communities (Rebman and
Roberts 2012). Bat roosts occurring in the mid-peninsular region
occurred in the Gulf coast ecoregion in habitats dominated by
spring- and summer-blooming columnar cacti, such as cardón
(P. pringlei) and organ pipe (Stenocereus thurberi, Cactaceae).
Bat roosts identified in the southern peninsula region occurred
in the sarcocaulescent shrubland ecoregion bordering tropical
dry forest (http://bajaflora.org/). Habitats near southern roosts
had high densities of columnar cacti dominated by the same
spring- and summer-blooming species (P. pringlei and S. thur-
beri) but also contained the cardón-barbón columnar cactus
(P. pecten-aboriginum, Cactaceae) that blooms November–
February. Agave species occurred in all ecoregions where bat
roosts were located but at lower densities and with less predict-
able flowering phenologies (Rebman and Roberts 2012; Webb
and Starr 2015).
Roost locations and seasonal use.—We identified existing
and new roost localities of lesser long-nosed bats on the Baja
peninsula by searching the literature, querying museum capture
records, and talking to local communities and other research-
ers. We visited 8 focal roosts in at least 3 of 4 seasons from
October 2013 through April 2016 (Figs. 1 and 2). Seasons were
defined as 3-month periods relating to general phenology of
nectar and fruit availability in the region: November–January
(low), February–April (nectar), May–July (nectar and fruit),
and August–October (fruit). We visually estimated the num-
ber of lesser long-nosed bats present and identified presence of
other species during surveys inside the focal roosts (Table 1).
Visual counts of lesser long-nosed bats are extremely challeng-
ing because the bats are active and fly readily when disturbed.
We initially took photographs of clusters of bats to estimate
density of individuals in a cluster and then approximated colony
size by extrapolating surface area by cluster density. We show
these approximated colony sizes in Fig. 2, but because colony
size estimates were imprecise, we used presence–absence of
bats at roosts in statistical analyses on seasonal patterns of roost
occupancy.
Passive integrated transponder tag monitoring.—We initi-
ated a long-term monitoring program using passive integrated
transponders (PIT tags) and installing Biomark IS1001 radio-
frequency identification transceivers attached to 15 m flexible
cord antennae (Biomark, Inc., Boise, Idaho) at 3 roost locations:
Fig. 2.—Seasonal patterns of roost occupancy at 8 roosts of lesser
long-nosed bats (Leptonycteris yerbabuenae) in Baja California Sur,
Mexico. Lines connect survey occasions sampled in consecutive sea-
sons. The Mulegé and Carmen roosts occur in the mid-peninsular
region and all other sites occur in the southern peninsula.
FRICK ET AL.—SEASONAL ECOLOGY OF A MIGRATORY BAT 1075
2 mines (Chivato and La Gitana) in the southern peninsula and
a natural cave (Isla Carmen Cave) in the mid-peninsular region
(Fig. 1). IS1001 readers were installed and continuous monitor-
ing commenced at the Chivato Mine in January 2015 and at the
La Gitana Mine in January 2017. We first marked bats with PIT
tags (see below) at the Carmen Cave in spring 2013, but due to
some early technical problems with an initial system, we were
unable to reliably collect data at this site until the system was
replaced in March 2015. We tagged 1,107 lesser long-nosed
bats from 6 different roost locations from 2013 to 2017, with
the majority of tagging occurring at the focal roosts Carmen
and Chivato (Table 2).
Bat capture and handling.—We captured bats by either plac-
ing harp traps at roost entrances or entering a site and using
hoop nets. We determined sex, age, and reproductive condition
and measured mass and forearm length of captured individuals
(Racey 2009). We marked bats with pit tags by subdermally
inserting a 12-mm tag premounted into a sterilized needle
loaded in an applicator gun (Biomark, Inc.) under the dorsal
skin (Kunz and Weise 2009). The insertion site was sealed using
a fast-acting medical adhesive (3M Vetbond Tissue Adhesive).
To determine reproductive timing at maternity sites, we
assessed reproductive condition of adult females and devel-
opment stage of young in early April. Young were classified
into 4 categories based on pelage and size characteristics cor-
responding to developmental stage (newborn, infant, juvenile,
and volant; see Supplementary Data SD1). Since females typ-
ically leave young inside the roost while foraging at night, we
assessed development stage class of young by waiting for adult
females to leave and visually surveying young inside the roost.
To minimize disturbance, we used red lights and visually clas-
sified as many young as possible in 15 min.
Research activities followed ASM guidelines (Sikes et al.
2016) and were approved by the UC Santa Cruz Institute of
Animal Care and Use Committee (IACUC) under protocol
Frickw1602. All necessary permits were issued by Dirección
General de Vida Silvestre, SEMARNAT, to RAM with collabo-
rative permissions to WFF.
Seasonal occupancy analysis.—To determine whether sea-
sonal occupancy patterns differed in mid-peninsular and south-
ern regions, we used generalized linear models with binomial
errors and the bias-reduction method (package brglm in R
v. 3.1.2) and fit 5 a priori candidate models with observed pres-
ence or absence of bats at a roost as the binary response and
region (mid-peninsula and southern peninsula) and season as
Table 1.—Description and protection status of 13 roosts of lesser long-nosed bats (Leptonycteris yerbabuenae) in Baja California Sur, Mexico.
Bold indicates roosts not previously reported; gray shading highlights roosts recently destroyed.
Site Feature Roost type Protection status Other bats present Region
Mina La JuliaaMine Seasonal stopover Unknown Choeronycteris mexicana
Myotis californicus
Northern Baja
San Sebastián Cave Seasonal stopover Unprotected, known by local ranchers Macrotus californicus Mid-Baja
Mulege Modified cave Maternity Unprotected, near town sprawl Macrotus californicus Mid-Baja
Coronados Sea cave Maternity Protected in National Park Myotis vivesi Gulf Island
Mid-Baja
Carmen Cave Maternity Protected on privately owned island Macrotus californicus Gulf Island
Mid-Baja
Mina San Jose Mine Maternity Destroyed after 2006 Macrotus californicus Gulf Island
Mid-Baja
Cueva de la Iglesia Cave Maternity Vandalized with fire and abandoned in 2018 Macrotus californicus
Myotis spp.
Southern Baja
Chivato Mine Mating and Maternity Protected on private ranch Macrotus californicus
Natalus mexicana
Southern Baja
La Gitana Mine Maternity Protected on private ranch Macrotus californicus Southern Baja
Azedon Mine Maternity Protected on private ranch Macrotus californicus Southern Baja
El Tesoro Mine Maternity Collapsed in 2015 Macrotus californicus
Natalus mexicana
Southern Baja
La Capilla Mine Maternity Destroyed in 2017 Macrotus californicus
Natalus mexicana
Mormoops megalophylla
Southern Baja
Las Cuevas Cave Mating and Maternity Unprotected, known by locals.
Pictures and location occasionally
posted online
Macrotus californicus
Tadarida brasiliensis
Myotis velifer peninsularis
Southern Baja
a Source: Guevara-Carrizales et al. (2010).
Table 2.—Total number of lesser long-nosed bats (Leptonycteris
yerbabuenae) marked with passive integrated transponder (PIT) tags
from 2013 to 2017 from 6 roost locations in Baja California Sur,
Mexico. Gray shading indicates years and sites with continuous active
monitoring with Biomark IS1001 transceivers.
Site Number of bats tagged Total
2013 2014 2015 2016 2017
Carmen 222 36 102 60 100 520
Chivato 207 57 57 321
La Gitana 47 96 143
Azedon 25 25
La Capilla 53 53
Las Cuevas 17 28 45
1076 JOURNAL OF MAMMALOGY
categorical predictors (Table 3). We used Akaike’s informa-
tion criteria (AIC) for model selection (Burnham and Anderson
2002). We also calculated the fraction of tagged bats from each
tagging occasion detected by roost antennae each day from
January 2015 to February 2018 at 2 focal roost sites in the mid-
and southern peninsula (Carmen and Chivato, respectively;
Fig. 3).
Reproductive timing and body mass of females.—We used
generalized linear models with binomial errors to test if the
probability that reproductive stage of adult females or young-of-
year development stage differed between regions for sites sam-
pled in early April to determine whether timing of reproduction
varied between the mid-peninsular and southern regions. In all
logistic regression analyses, we used a bias-reduction method
(package brglm in R v. 3.1.2) to deal with complete separation
present in the data. We used a general linear regression with
body mass as response and a categorical predictor of reproduc-
tive status with 5 categories (nonreproductive, pregnant, lactat-
ing, lactating and carrying pup, and post-lactating) to describe
body mass changes in females associated with reproduction.
We were unable to test for seasonal effects on body mass of
females because changes in body mass of females related to
reproduction were confounded with seasons.
Seasonal variation in body mass and reproductive sta-
tus of males.—We captured male lesser long-nosed bats in
all seasons in the southern peninsula and used general linear
regression with body mass as the response variable and sea-
son as a categorical explanatory variable to test whether body
mass of males varied seasonally. We predicted that bats would
have higher body mass in seasons corresponding to when the
dominant columnar cacti (e.g., P. pringlei) are in flower and
fruit in the region (March to July). Male bats were scored as
reproductively active if their testes were swollen and distended
Table 3.—Model comparison for seasonal roost occupancy logistic
regression. Models were fit with a binomial distribution and a logit
link using a bias-reduction method implemented in the brglm function
from package brglm in program R. ΔAIC = difference in Akaike’s
information criterion value between the focal model and the top-
ranked model in the set. AIC weight = the relative likelihood of the
focal model.
Model structure ΔAIC AIC weights
Logit(Pr(Occupancy)) ~
Season 0 0.65
Season + region 1.35 0.33
Season * region 8.59 0.01
1 (null) 9.92 0.00
Region 11.57 0.00
Fig. 3.—Patterns of seasonal occupancy at the Isla Carmen maternity roost in mid-Baja (A) and the Chivato maternity and mating roost in south-
ern Baja (B) from daily detections of bats marked with pit tags passing through antennae at roost entrances. Gray boxes indicate periods when the
tag reader was not functioning.
FRICK ET AL.—SEASONAL ECOLOGY OF A MIGRATORY BAT 1077
(Racey 1988; Ceballos et al. 1997; Stoner et al. 2003). Male
lesser long-nosed bats develop a sebaceous patch in the inter-
scapular dorsal region during mating season (Nassar et al.
2008; Rincón-Vargas et al. 2013). We noted presence of this
distinctive patch as well as discolored fur in the middorsal area
indicating recent molting and regrowth of fur from a sebaceous
patch (Nassar et al. 2008).
results
Distributional records and roost status.—We report a total of
13 roost sites of lesser long-nosed bats on the Baja peninsula,
including discovery of 10 roosts not previously reported in the
literature (Table 1). Eight of these roosts were visited in multi-
ple seasons as part of this study (Fig. 1). We discovered 2 pre-
dominately male roosts in the southern peninsula (Las Cuevas
and Chivato Mine; Fig. 1) and confirmed males were in mating
condition at these roosts in autumn, documenting evidence of
mating sites for lesser long-nosed bats on the Baja peninsula.
We documented the intentional destruction or natural collapse
of 3 maternity roosts of lesser long-nosed bats, representing a
loss of almost one-third of the known maternity roosts of the
species on the peninsula (Table 1).
Seasonal occupancy.—Probability of roost occupancy dif-
fered among seasons on the Baja peninsula, but there was not
strong support for regional differences in seasonal patterns of
roost occupancy (Tables 3 and 4). Occupancy in winter was
significantly lower than in spring or summer (P < 0.04) in both
regions (Fig. 2). Three sites in close proximity to each other
(< 15 km) in the Sierra Cacachilas in the southern peninsula
had bats present in some winters: 2 sites used as maternity
roosts (Azedon, La Gitana) had less than 100 bats present
(< 1% of their spring population) and the Chivato roost used for
maternity and mating had between 10 and 1,000 individuals in
winter (numbers varied by 2 orders of magnitude depending on
year but was always < 10% of its spring–summer–fall popula-
tion; Figs. 2 and 3).
Bats marked with pit tags were detected daily at the Carmen
maternity roost from mid-March to mid-July (Fig. 3A),
closely corresponding to the seasonal phenology of flower-
ing and fruiting of cardón cacti (Fleming et al. 2001). In
contrast, tagged bats were detected nearly year-round at the
Chivato roost, although very few bats were detected from
November to mid-February (Fig. 3B). At both sites, daily
detections of tagged bats were substantially higher in the
season they were initially tagged than in following seasons.
At Chivato, the fraction of daily detections was consistently
lower for bats tagged during January, suggesting the major-
ity of bats using the site during mid-winter migrate else-
where in other seasons (Fig. 3B).
Reproductive timing and body mass of females.—Timing of
parturition at maternity colonies occurred significantly earlier
in the year at southern compared to mid-peninsular regions
(Fig. 4). In early April, the proportions of newborn and infant
stage classes and proportion of females still pregnant were sig-
nificantly higher (P < 0.001) in the mid-peninsula than in the
southern peninsula (Table 5; Fig. 4). Conversely, in early April
the proportions of pre-volant and volant young and adult females
who were lactating were significantly higher (P < 0.001) in the
south than the mid-peninsula (Table 5; Fig. 4). Young were
Table 4.—Estimated model coefficients and SEs for 2 top-ranked
models based on Akaike’s information criteria (AIC) model selection
for seasonal roost occupancy of lesser long-nosed bats (Leptonycteris
yerbabuenae) on the Baja California peninsula. Although the model
with region had competing support based on AIC, the regional term
was not significant (P = 0.41).
Model term Coefficient SE Z-value P-value
Pr(Occupancy) ~ season
Intercept (reference = winter) −0.96 0.79 −1.21 0.23
Season: spring 3.79 1.73 2.19 0.03
Season: summer 3.66 1.75 2.09 0.04
Season: autumn 1.41 1.07 1.31 0.19
Pr(Occupancy) ~ season + region
Intercept (reference = winter and southern) −0.72 0.81 −0.88 0.38
Season: spring 3.77 1.71 2.20 0.03
Season: summer 3.68 1.74 2.12 0.03
Season: autumn 1.42 1.09 1.30 0.19
Region: mid-peninsula −0.93 1.12 −0.83 0.41
Fig. 4.—Proportion of reproductive and age classes sampled in early
April at 5 maternity sites of lesser long-nosed bats (Leptonyteris yerb-
abuenae) on the Baja California peninsula. The proportion of preg-
nant females and young that were newborn or infants was significantly
higher in the mid-peninsular region than in the south (Table 3), sug-
gesting that timing of parturition occurred later at sites in the mid-
peninsula compared to the southern peninsula.
1078 JOURNAL OF MAMMALOGY
observed starting in mid-February in the south, about 2 months
earlier than at mid-peninsula sites.
Pregnant females captured between February and April
weighed an average 31 g (SE = 0.23), which was an average
37% greater body mass compared to nonreproductive females
captured in those months (Fig. 5). Females captured and
weighed carrying pups were 10 g (SE = 0.46) heavier than lac-
tating females without pups (23.7 g, SE = 0.12), demonstrating
that females were capable of carrying young weighing 44% of
their own body mass. We note that we only captured females
carrying young inside a roost or moving to a nearby night roost,
indicating females do not likely carry young while traveling
long distances during foraging bouts.
Seasonal variation in body mass and reproductive status
of males.—Body mass of male lesser long-nosed bats peaked
in spring and summer months, coinciding with availability
of columnar cacti nectar and fruit availability (Fig. 6). Male
bats weighed an average of 27 g in February–April and
May–July (Fig. 6), which was 2 g heavier than the average
weight of males (25 g) in August–October and November–
January. The 2 g increase in body mass from autumn and
winter to spring and summer indicates an 8% increase in
body mass across seasons. Although adult males with dis-
tended and swollen testes were captured in all seasons,
there were clear seasonal patterns to reproductive status of
males in the southern peninsula. Ninety-four percentage
of adult males captured in July had distended and swol-
len testes (n = 65/69) compared to only 10% (n = 13/128)
captured during mid-winter (December–January; Fig. 6).
Almost all adult males captured in early October at Las
Cuevas (n = 9/10) in 2013 and 61% of adult males cap-
tured at Chivato in September 2017 (n = 11/18) had active
sebaceous patches (bare dorsal skin with sticky fur). About
one-half the adult males (n = 6/15) captured in mid-October
at Chivato in 2016 had bare dorsal skin with regenerating
fur suggestive of just finishing mating. In mid-winter visits
to Chivato from 2014 to 2016, nearly 43% of adult males
captured (n = 55/128) had newly grown fur that was distinct
in coloration in the area where the dorsal sebaceous patch
forms, suggesting these males had been in breeding condi-
tion in previous months.
Table 5.—Estimated model coefficients and SEs for logistic regres-
sion models fit to test whether reproductive timing differed by region
for lesser long-nosed bats (Leptonycteris yerbabuenae) on the Baja
California peninsula. Models were fit for each reproductive class
(pregnant, lactating) or development stage of young (newborn, infant,
pre-volant juvenile, volant juvenile). All models were fit with a bino-
mial distribution and a logit link using a bias-reduction method imple-
mented in the brglm function from package brglm in program R.
Model Coefficient SE Z-value P-value
Adult females
Pr(Pregnant) ~ region
Intercept (reference = southern) −3.07 0.55 −5.82 < 0.001
Region: mid-peninsula 3.26 0.58 5.82 < 0.001
Pr(Lactating) ~ region
Intercept (reference = southern) 2.12 0.37 5.79 < 0.001
Region: mid-peninsula −3.36 0.43 −7.73 < 0.001
Young-of-the-year
Pr(Newborn) ~ region
Intercept (reference = southern) −3.32 0.43 −7.63 < 0.001
Region: mid-peninsula 4.08 0.47 8.61 < 0.001
Pr(Infant) ~ region
Intercept (reference = southern) −1.69 0.22 −7.69 < 0.001
Region: mid-peninsula 0.90 0.29 3.12 < 0.01
Pr(Pre-volant) ~ region
Intercept (reference = southern) −0.32 0.16 −1.97 0.05
Region: mid-peninsula −4.15 0.84 −4.95 < 0.001
Pr(Volant) ~ region
Intercept (reference = southern) −0.42 0.16 −2.60 < 0.001
Region: mid-peninsula −5.16 1.4 −3.6 < 0.001
Fig. 5.—Differences in body mass of female lesser long-nosed
bats (Leptonycteris yerbabuenae) on the Baja California peninsula.
Lactating females that were weighed carrying pups are shown as a
separate group. Boxplots are notched to show median and quartiles,
and black diamonds show means. Letters denote groups that were sig-
nificantly different based on Tukey’s method for post hoc contrasts.
Fig. 6.—Changes in body mass across seasons for male lesser long-
nosed bats (Leptonycteris yerbabuenae) in the southern Baja California
peninsula, Mexico. Males were scored as reproductively active if tes-
tes were distended and swollen. Boxplots are notched to show median
and quartiles, and black diamonds show means. Letters denote groups
that were significantly different based on Tukey’s method for post hoc
contrasts. Seasonal changes in relative colony size for the Chivato
mating roost are shown at top.
FRICK ET AL.—SEASONAL ECOLOGY OF A MIGRATORY BAT 1079
discussion
We provide evidence of an extensive population of lesser long-
nosed bats on the Baja peninsula that is primarily seasonally
migratory and includes at least 2 mating sites with males in
active breeding condition in the southern peninsula. We found
that most female lesser long-nosed bats present on the Baja pen-
insula use it during the spring and summer to give birth and raise
young, a seasonal pattern similar to migratory maternity roosts
studied in the northern mainland Sonoran Desert and southwest-
ern United States (Rojas-Martínez et al. 1999). However, some
females arrived to give birth at maternity sites in the southern
peninsula by mid-February, which is about 2 months earlier than
in mid-Baja and northern Sonoran Desert regions. A mating
roost in the southern peninsula retained small numbers of both
males and females, including some pregnant females, during
mid-winter. Except for this small population, lesser long-nosed
bats were largely absent from all maternity sites on the Baja
peninsula during mid-winter in both the southern and mid-pen-
insular regions. Our data suggest that the majority of the popu-
lation of lesser long-nosed bats on the Baja peninsula, including
both males and females, migrate over the Gulf of California to
the Mexican mainland rather than overwinter in the southern
peninsula as had been previously suggested.
The presence of winter-blooming agaves in the southern pen-
insula has been suggested as a food resource for lesser long-
nosed bats that overwinter in the Cape region of Baja (Fleming
et al. 1993). While there are 22 species of agave that occur on
the Baja peninsula, only 3 species are found in the southern
peninsular Cape region (Webb and Starr 2015). Two of these
species typically bloom in the spring months from roughly
February to April and the other has a typical autumn bloom per-
iod from September to December (Rebman and Roberts 2012).
Flowering seasons of agaves are more variable and less sea-
sonally predictable than those of columnar cacti and are likely
highly influenced by climatic events, such as droughts or hur-
ricanes (R. H. Webb, University of Arizona, pers. comm.). The
unpredictability of agave flowering and overall low density of
agaves in the region make it unlikely that agaves provide a reli-
able or substantial food source for a large population of lesser
long-nosed bats during winter months in southern Baja. Our
data show that the population of lesser long-nosed bats in Baja
swells significantly when columnar cacti are flowering and
fruiting and only a small fraction of that population remains
in the area during mid-winter when nectar and fruit resources
are at their lowest availability. Both males and females leave
the region when resources are scarce. However, surprisingly,
we found that some females began arriving at a few of the
maternity sites in the southern peninsula in late stages of preg-
nancy to give birth by mid-February, which is 2 months earlier
than when parturition typically occurs at more northern sites
and before the onset or peak of flowering of cardón cacti. Two
agave species and the cardón-barbón (P. pecten-aboriginum), a
columnar cactus restricted to the eastern cape of Baja, bloom
during February (Rebman and Roberts 2012), which may pro-
vide enough floral resources for a shift in birthing phenology at
sites in the southern peninsula.
The seasonal ecology of lesser long-nosed bats appears to
be primarily driven by the flowering and fruiting season of
the cardón, the dominant columnar cactus on the peninsula
(Rebman and Roberts 2012). Parturition was synchronous and
timed with onset of flowering at mid-peninsular roosts and
although some females arrived in mid-February to southern
roosts, there was a second birthing pulse during onset of flower-
ing of cardón at those sites as well (Fig. 4). Body mass of males
increased on average by 8% during the flowering and fruiting
season of cardón and males had obvious ample fat reserves by
July. Although we could not test for seasonal effects on body
mass of females due to the confounding effects of pregnancy
on body mass during spring, we note that females showed up
to maternity sites on the Baja peninsula in mid- to late stages
of pregnancy, a period when females are carrying a nearly 40%
increase in mass. Arriving from migration in late pregnancy
suggests females will be at peak energetic demand when they
arrive at maternity roosts and shifts in flowering phenology
or availability of dominant food resources could pose risks to
these populations (Memmott et al. 2007).
Daily detections of marked bats at pit tag readers at the
Carmen and Chivato roosts revealed differences in seasonal
use and patterns of behavior. At Carmen, bats arrived synchro-
nously in March and departed synchronously in early August,
with no bats present until the following March. In addition, in
both 2016 and 2017, the majority of tagged bats departed the
roost for about 2 weeks in early June. Early June coincides with
when the flowering season of the cardón has largely ended but
the majority of fruit are not yet ripe (W. F. Frick, pers. obs.).
This may be when resource availability is shifting and bats
begin exploring new areas. In contrast, the Chivato roost had
some bats present year-round in most years, although occu-
pancy was highest from mid-February to mid-November. Bats
departed en masse from Chivato in November 2015, but less
synchronously in 2016.
Bats tagged at the Carmen roost showed high fidelity and
typically > 75% of tagged bats were detected using the site each
day in the same season they were tagged. At Chivato, compara-
ble levels of same-season fidelity were only observed for male
bats tagged in July 2015. A few factors could influence lower
fractions of daily detections of tagged bats at Chivato. Firstly,
Chivato is located very near 2 maternity roosts (< 1 km from
La Gitana and < 15 km from Azedon), so bats can easily switch
roosts on a nightly basis. We deployed an additional reader at
the La Gitana roost entrance in January 2017 and preliminary
data suggest roost switching is very common with both male
and female bats routinely moving back and forth between the
sites. Moreover, patterns of daily detections differed for bats
tagged in different seasons and less than a quarter of bats
tagged in January used the site consistently, suggesting that the
majority of bats using Chivato in mid-winter are not resident
year-round but are instead likely migrants.
Lesser long-nosed bats are particularly vulnerable to dis-
turbance at roosts given that they roost in large aggregations
in caves and mines (Medellín 2009; Medellín et al. 2017).
Protection of maternity sites is a critical conservation strategy
1080 JOURNAL OF MAMMALOGY
for the species and is generally needed for conservation of
cave-dwelling bats (USFWS 1995; Medellín et al. 2017).
Many of the roost sites we studied on the Baja peninsula are
unprotected and vulnerable to future and current disturbance.
During our surveys, we discovered 3 maternity roost sites
(nearly 1/3 of known maternity sites) were destroyed, 1 by
natural causes and the other 2 by deliberate action. The Tesoro
mine, which held roughly 10–20,000 lesser long-nosed bats
as well as substantial numbers of California leaf-nosed bats
(Macrotus californicus) and Mexican funnel-eared bats
(Natalus mexicana), likely collapsed during an earthquake in
September 2015 (Table 1). The earthquake occurred at night
and it remains unknown how many bats may have been killed
as a result. A mine on Isla San Jose that held thousands of
lesser long-nosed bats and hundreds of California leaf-nosed
bats in May of 2006 was bulldozed and closed. We were una-
ble to obtain details as to when the shaft was closed but if it
occurred during April–June, it is likely that thousands of bats
were killed as a result. Similarly, the La Capilla roost that was
a maternity colony for 4 species, including lesser long-nosed
bats, Mexican funnel-eared bats, ghost-faced bats (Mormoops
megalophylla), and California leaf-nosed bats (Table 1),
was bulldozed closed sometime in 2017. In April 2018, we
confirmed that an additional roost known by PC-C near the
university campus in La Paz (Cueva de la Iglesia; Table 1)
had been vandalized with use of fire and the bats had aban-
doned the site. Conservation efforts to inform locals residing
nearby substantial roosts of lesser long-nosed bats and other
cavernicolous bat species could help reduce human–wildlife
conflicts and support protection of these colonies as has been
successful in other parts of Mexico (Medellín 2003, 2009;
Medellín et al. 2004). Most remaining known maternity colo-
nies in the southern peninsula occur on a private ranch that is
committed to the protection of the bats.
Although the Baja peninsula is separated from mainland
Mexico by the Gulf of California, habitats on the Baja pen-
insula support an extensive population of lesser long-nosed
bats that is primarily seasonally migratory and closely
linked to the seasonal phenology of columnar cacti. Genetic
analyses support that lesser long-nosed bats on the Baja
peninsula are connected and that the population expanded
into the Baja peninsula following the Pleistocene when food
resources became available (Ramirez 2011; Arteaga et al.
2018). Overall, our data support the decision to delist the
lesser long-nosed bat from endangered and threatened status
in both the United States and Mexico. However, we note that
legally and effectively protecting roost sites from deliberate
destruction and monitoring populations, including those on
the Baja peninsula, will be critical for ensuring the contin-
ued persistence of the species. Habitats on the Baja penin-
sula are at high risk of environmental change both from land
use and climate change (Zamora-Gutierrez et al. 2018), and
migratory nectar-feeding bats are particularly vulnerable to
global changes that affect availability and predictability of
seasonal nectar and fruit resources (Medellín et al. 2004;
Medellín 2009).
acknowledgMents
We thank J. Flanders for comments on an earlier draft. We
thank Parque Nacional Bahía de Loreto, Organización Vida
Silvestre, AC (OVIS) and Rancho Cacachilas for hospitality
and support of this research and for protecting important roost
sites. We thank A. Esliman, R. Jackson, T. Haglund, E. Israel
Popoca Arellano, and the team at the San Diego Natural
History Museum. Many people assisted with fieldwork for this
project, including Q. Frick, C. Larson, M. Landon, R. Bathrick,
S. Chavez, S. Klinefelter, H. Rogers, A. Ananda, A. Froschauer,
J. Aliperti, and M. Baker. Funding was provided by UCMexus-
Conacyt, UNAM, International Community Foundation, and
Bat Conservation Research and Services. We thank A. Ibarra
for logistical support and Dirección General de Vida Silvestre,
SEMARNAT, for collecting permits.
suppleMentary data
Supplementary data are available at Journal of Mammalogy
online.
Supplementary Data SD1.—Photographic key to visual clas-
sification of developmental stage class of young-of-year lesser
long-nosed bats (Leptonycteris yerbabuenae).
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Submitted 20 April 2018. Accepted 12 July 2018.
Associate Editor was Jorge Ortega.
