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Interest in the Florida bonneted bat (Eumops floridanus) has risen dramatically since the species was listed as federally endangered in 2013. However, understanding of many aspects of the species’ biology is limited, due in part to the fairly recent recognition of E. floridanus as a distinct species rather than a subspecies of E. glaucinus. Through a two-year mark-recapture study of E. floridanus roosting in a group of bat houses, we obtained morphological measurements on .200 individuals. We documented modest male-biased sexual size dimorphism (forearm length, wing width, and wing length were larger in adult males than adult females) and found gular glands exclusively among males. If these morphological differences lead to niche partitioning between sexes, conservation planning may need to consider the foraging habitat use of males and females independently. Relative to other species in the genus Eumops, E. floridanus had a moderate aspect ratio index, low wing shape index, and low wing tip index, suggesting the species may not be capable of flying at speeds as fast as other closely related species, but may be more maneuverable and more efficient when flying in cluttered space.
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Biological Sciences
Sexual dimorphism in the endangered Florida bonneted bat, Eumops
floridanus (Chiroptera: Molossidae)
Holly K. Ober
(1)
, Elizabeth C. Braun de Torrez
(2)
, Robert A. McCleery
(2)
,
Amanda M. Bailey
(2)
, Jeffery A. Gore
(3)
(1)
Department of Wildlife Ecology and Conservation, University of Florida, 155 Research Road,
Quincy, FL 32351 USA
(2)
Department of Wildlife Ecology and Conservation, University of Florida, P.O. Box 110430,
Gainesville, FL 32611 USA
(3)
Florida Fish and Wildlife Conservation Commission, 3911 Hwy 2321, Panama City, FL 32409
USA
Abstract Interest in the Florida bonneted bat (Eumops floridanus) has risen dramatically since the
species was listed as federally endangered in 2013. However, understanding of many aspects of the
species’ biology is limited, due in part to the fairly recent recognition of E. floridanus as a distinct
species rather than a subspecies of E. glaucinus. Through a two-year mark-recapture study of E.
floridanus roosting in a group of bat houses, we obtained morphological measurements on .200
individuals. We documented modest male-biased sexual size dimorphism (forearm length, wing
width, and wing length were larger in adult males than adult females) and found gular glands
exclusively among males. If these morphological differences lead to niche partitioning between
sexes, conservation planning may need to consider the foraging habitat use of males and females
independently. Relative to other species in the genus Eumops,E. floridanus had a moderate aspect
ratio index, low wing shape index, and low wing tip index, suggesting the species may not be capable
of flying at speeds as fast as other closely related species, but may be more maneuverable and more
efficient when flying in cluttered space.
Keywords: Body condition, Eumops floridanus, Florida bonneted bat, morphology, sexual
dimorphism, wing shape
Introduction
The Florida bonneted bat (Eumops floridanus) is a rare species endemic to South
Florida, designated as federally endangered in 2013 (USFWS 2013). Eumops
floridanus is one of only eight species of the family Molossidae (free-tailed bats;
Norberg and Rayner 1987) found within the United States, and the only with
federal conservation status. Due to its rarity, small geographic range, and fairly
recent recognition as a distinct species (Timm and Genoways 2004), extremely
little is known about the basic biology of E. floridanus. A single species, E.
glaucinus, was previously believed to range across the northern one-third of South
America, Central America, Jamaica, Cuba, and south Florida (Barbour and Davis
1969). In recognition of significant morphological differences, Eumops occurring in
Corresponding author: Holly Ober, holly.ober@ufl.edu
38
Florida were designated a distinct subspecies in 1971 (E. g. floridanus; Koopman
1971), and then a distinct species in 2004 (E. floridanus; Timm and Genoways
2004). The recent classification of E. floridanus as an endangered species greatly
increases the need to understand its ecology (FWC 2011, USFWS 2013).
Establishment of baseline morphological data for E. floridanus is needed to
provide a foundation for future comparative studies and for developing appropriate
conservation strategies.
Although male-biased sexual dimorphism in body mass or size is relatively
common among many species of mammals (i.e., males are heavier or larger than
females; Isaac 2005), female-biased sexual dimorphism tends to be more pervasive
within Chiroptera (Ralls 1977, Williams and Findley 1979). For example, female-
biased sexual dimorphism is widespread among many species in the family
Vespertilionidae (Myers 1978, Williams and Findley 1979), particularly in forearm
length (Stevens and Platt 2015). In contrast, Molossidae commonly exhibit male-
biased sexual dimorphism (Freeman 1981). Male-biased sexual dimorphism has
been reported in several species of Eumops (Eger 1977), with more pronounced
differences in larger species within the genus. Eumops floridanus is intermediate in
overall size among these species, and the occurrence of sexual dimorphism in E.
floridanus is uncertain. The few studies that have investigated sexual dimorphism in
the closely related E. glaucinus have reached mixed conclusions regarding
dimorphism in mass and forearm length (Gardner et al. 1970, Eger 1977, Silva
Taboada 1979, Myers and Wetzel 1983, Bowles et al. 1990). Understanding
patterns of sexual dimorphism can be critical to development of species-specific
conservation strategies if differences in morphology result in differential habitat
selection or movement patterns between sexes (Blanckenhorn 2005, Isaac 2005).
Wing morphology is the primary determinant of flight capabilities of bats,
affecting foraging strategies, extent of foraging area, and migratory capacity
(Fenton 1972, Findley et al. 1972, Norberg 1972). Wing shapes vary among species
and also between sexes within species, resulting in differential habitat selection,
movement patterns, time budgets, diet, thermoregulatory requirements, metabolic
rates, and susceptibility to predation (Ralls 1977, Blanckenhorn 2005, Isaac 2005).
Wing length, wing tip length, aspect ratio, and speed are high among species in
Molossidae (Findley et al. 1972), whereas wing area is relatively small (Norberg
and Rayner 1987). Bats with long, narrow wings generally have rapid, efficient
flight, whereas bats with short broad wings have high turning performance (i.e.,
high maneuverability, meaning a small minimum space is required to change flight
directions at a given speed, and high agility, meaning a turn can be initiated at a
rapid rate; Findley et al. 1972, Norberg 1972). Molossids use swift, direct flight
trajectories to pursue prey through aerial hawking in open habitats or at high
altitudes, and to fly long distances when commuting between roosts and foraging
areas or migrating (Findley et al. 1972, Freeman 1981, Aldridge and Rautenbach
1987, Norberg and Rayner 1987). High metabolic costs are incurred when these
bats attempt to fly at slower speeds in confined spaces relative to faster speeds in
straight flight, which may constrain many molossids to forage exclusively in open
environments (Voigt and Holderied 2012). Gradation in flight capabilities among
Dimorphism in Eumops floridanus Ober et al.
Florida Scientist 80(1) 2017 QFlorida Academy of Sciences 39
species within Molossidae can be predicted on the basis of wing morphology
(Freeman 1981). To date, few live E. floridanus individuals have been captured,
and morphological measurements of E. floridanus specimens are extremely scarce.
Nothing is known about sexual dimorphism in wing morphology, or about wing
shape relative to that of closely-related species, constraining our understanding of
flight capabilities of these bats.
Due to a lack of data on basic morphology and flight capacity in E. floridanus,
our goal was to obtain a robust dataset of morphological measurements that would
enable interspecific and intraspecific comparisons. Given the presence of male-
biased sexual dimorphism in other Eumops and the ecological implications of
variation in wing morphology, our objectives were to compare mass, size, body
condition and wing morphology in E. floridanus of different sexes and ages, and
contrast wing morphology with that of other Eumops species.
Materials and Methods
We conducted this study at Fred C. Babcock - Cecil M. Webb Wildlife Management Area (BWWMA) in
southwest Florida. The vegetation communities were a mix of mesic and hydric pine flatwoods with
embedded freshwater marshes, ponds, and hardwood hammocks. Average annual temperature was
23.48C, and average rainfall was 128.8 cm per year, most of which fell during summer months (http://
www.usclimatedata.com). BWWMA was owned and managed by the Florida Fish and Wildlife
Conservation Commission (FWC).
Eumops floridanus was observed in Punta Gorda, FL (5 km from BWWMA) in 1979 (Belwood
1981), and was first detected on BWWMA in 2006. To augment roosting habitat for the species, the
FWC erected matched pairs of one- or three-chamber bat houses on poles at eight sites in 2007-2008, and
at five additional sites in 2012. Each pair of bat houses sharing a pole is considered a single roost. To
date, E. floridanus have been observed in nine of these 13 roosts.
We conducted seven multi-day capture sessions spaced four months apart: 22-25 April 2014, 27-30
August 2014, 15-17 December 2014, 20-24 April 2015, 24-26 August 2015, 14-16 December 2015, and
19-21 April 2016. During each session, we used triple-high mist nets in an attempt to catch every E.
floridanus roosting in each of the occupied roosts. Mist nets were opened at sunset and remained open for
a maximum of three hours.
Each captured bat was placed individually in a numbered cotton bag, and examined to determine
age (adult/sub-adult), sex, body mass, forearm length, reproductive status, and the presence or absence of
gular-thoracic glands. Sub-adults were distinguished from adults by examining the degree of fusion of
phalangeal cartilage; when that was ambiguous, we used status of genitals and mammae as secondary
indicators of age. Adult females were classified as non-reproductive, pregnant, lactating, or post-
lactating. Adult males were classified as non-reproductive (testes abdominal) or reproductive (testes
descended). We calculated body condition index (BCI ¼mass/forearm length; Reynolds et al. 2009,
Jonasson and Willis 2011, Lis´
on et al. 2014) to generate a relative metric of each bat’s overall condition
and to facilitate future comparisons of mass relative to body size when making inferences about wing
loading and fat reserves among individuals of different ages, sexes, and reproductive status.
During the December 2015 and April 2016 capture sessions, we took four additional wing
measurements from a subset of individuals. We fully extended the right wing of each bat and measured
the following lengths using dial calipers (precision 60.1mm): the distance from the wrist to the tip of
the 5
th
finger excluding the wrist (D5), distance from the wrist to the tip of the 3
rd
finger excluding the
wrist (D3), and length of the 1
st
and 2
nd
phalanx of the 4
th
finger (Figure 1). These are considered simple
descriptions of wing width (D5), wing length (D3), and wingtip width (1
st
and 2
nd
phalanx of the 4
th
finger; features that vary greatly in length among Molossidae; Freeman 1981). Each measurement was
repeated three times by the same observer and averaged. From these measurements we calculated three
indices: aspect ratio index ([D3þforearm]/D5; Findley et al. 1972), wing shape index (D3/D5; Fenton
Ober et al. Dimorphism in Eumops floridanus
40 Florida Scientist 80(1) 2017 QFlorida Academy of Sciences
1972), and tip index (100*D3/[D3þforearm]; adapted by Freeman 1981), to facilitate comparisons with
wing shapes of other Eumops species.
All bats were uniquely marked with passive integrated transponders (PIT-tag; 12 mm, 134.2 kHz
FDXB tags (Biomark Inc., Boise, ID)) to enable identification of recaptured individuals. Tags were
implanted subcutaneously in the lower lumbar region near the plagiopatagium. After processing, each bat
was released near the site of capture. All capture and handling processes followed American Society of
Mammalogists guidelines (Sikes et al. 2011), were approved by the University of Florida IACUC
(#201308070 and 201408587), and were in accordance with U.S. Fish and Wildlife Service permit #TE
23583B-1 and Florida Fish and Wildlife Conservation Commission permit #SUO-49616.
After examining all data to determine whether assumptions of normality and homogeneity of
variance were met with Shapiro-Wilks and Levene’s tests, we tested for differences in morphometric
measurements between sexes (mass and forearm length) using student’s t-tests (when data met
assumptions of normality and homogeneity of variance), Welch’s t-tests (when data had unequal
variance), or Mann-Whitney U tests (when data were not normally distributed). We tested for differences
in wing metrics (D5, D3, 1
st
and 2
nd
phalanx of the 4
th
finger) using MANOVA. Lastly, we compared
measurements among individuals of different reproductive status categories using ANOVA followed by
Tukey HSD tests for multiple comparisons. For all morphometric comparisons involving individuals
captured more than once, we used a single mean value to represent each characteristic for each individual
that was reported in the same reproductive category during more than one capture session. Throughout,
we define sexual size dimorphism as any statistically significant difference in morphometric
measurements of different sexes within the same age or reproductive category (Lovich and Gibbons
1992). All statistical analyses were conducted with SPSS version 23.0 (IBM Corp. 2015).
Results
During each of the seven capture sessions we captured 50, 61, 42, 56, 63, 79, and 89
individual Eumops floridanus respectively. In total we captured 201 unique
individuals: 36% were males and 64% were females. Gular glands were apparent on
all adult males and most sub-adult males, but absent from all females of both age
groups.
Mass ranged greatly among individuals (from 27 to 59 g), but we did not find
sexual dimorphism in mass (Table 1). Mass of all adult males (n¼65) did not differ
from mass of adult females that were not pregnant (i.e., non-reproductive or post-
lactating, n¼109) (t
172
¼0.090, p¼0.928). Similarly, mass of non-reproductively
Figure 1. Diagram showing measurements used to reflect Eumops floridanus wing size and shape.
Dimorphism in Eumops floridanus Ober et al.
Florida Scientist 80(1) 2017 QFlorida Academy of Sciences 41
active adult males (n¼16) did not differ from mass of non-reproductively active
adult females (n¼50) (t
18.26
¼0.137, p¼0.893).
We detected male-biased sexual dimorphism in forearm length, a characteristic
typically used to reflect overall body size in bats (Table 1). Forearm length ranged
from 60.0 to 69.1 mm. Forearm length of all adult males (¯
x¼63.74 61.44 mm, n¼
54) was significantly greater than that of all adult females (¯
x¼62.74 61.23 mm, n
¼111) (t
163
¼4.642, p,0.001). Similarly, forearm length of sub-adult males
(median ¼63.3 mm, n¼35) was significantly greater than that of sub-adult females
(median ¼62.5 mm, n¼35) (U ¼374.5, p¼0.005).
We found differences between adult males (n¼29) and females (n¼38) in
wing morphology (F
4,62
¼4.07, p¼0.005, Wilk’s K¼0.792, partial n
2
¼0.208).
Two of the four wing measurements differed between sexes, after Bonferroni
corrections to account for multiple comparisons (Table 2). Wing width (D5) was
greater in males than females (F
1,65
¼45.32, p,0.005; ¯
xdifference ¼1.56 mm,
95% CI from 0.76 to 2.35 mm larger). Wing length (D3) was also greater in males
than females (F
1,65
¼8.447, p¼0.005; ¯
xdifference ¼2.09 mm, 95% CI from 0.65
to 3.52 mm larger). In contrast, there were no differences in wingtip width (1st and
2
nd
phalanx of the 4th finger). Length of the first phalanx was similar in males and
females (F
1,65
¼4.1, p¼0.047; ¯
xdifference ¼0.44 mm, 95% CI from 0.01 to
0.87mm larger), as was length of the 2
nd
phalanx (F
1,65
¼0.007, p¼0.936; ¯
x
difference ¼0.01 mm, 95% CI from 0.02 mm smaller to 0.23 mm larger).
Body condition index (BCI) ranged from 0.460 to 0.952 (Table 1, Figure 2). We
found differences in BCI among bats of different reproductive categories [F
6, 274
¼
40.238, p,0.001]. There were no significant differences in BCI for post-hoc pair-
wise comparisons between male sub-adults, female sub-adults, male non-reproduc-
tive adults, and female non-reproductive adults; however, there were significant
differences in BCI for pair-wise comparisons between these categories and BCI of
reproductively active adult males, post-lactating females, and pregnant females.
Relative to seven other species in the genus Eumops,E. floridanus wing
morphology was typical in some respects but unusual in others. Eumops floridanus
had a moderate aspect ratio index, the second lowest wing shape index, and the
lowest tip index (Table 2).
Table 1. Mean (6SD) mass, forearm length, and body condition index (BCI; mass/forearm length) of
201 Eumops floridanus at Fred C. Babcock - Cecil M. Webb Wildlife Management Area, FL. Total
sample size exceeds the number of unique individuals captured because some individuals captured
multiple times exhibited different reproductive status during different capture events.
Sex Status nMass (g) Forearm (mm) BCI
Male reproductively active adult 31 43.77 64.38 63.72 61.49 0.686 60.062
non-reproductive adult 16 40.68 65.79 63.37 61.80 0.642 60.088
non-reproductive sub-adult 35 38.46 63.82 63.19 61.81 0.608 60.053
Female pregnant adult 56 47.13 64.10 62.75 61.30 0.750 60.063
post-lactating adult 59 45.29 62.96 62.79 61.26 0.722 60.046
non-reproductive adult 46 40.47 63.32 62.70 61.23 0.645 60.053
non-reproductive sub-adult 35 38.03 64.03 62.39 61.26 0.609 60.059
Ober et al. Dimorphism in Eumops floridanus
42 Florida Scientist 80(1) 2017 QFlorida Academy of Sciences
Table 2. Comparisons of selected wing characteristics among Eumops floridanus (mean 6SD, derived from this study) and those reported for other species in the genus
Eumops (from Freeman 1981).
Species nD3 D5 1
st
Phalanx of D4 2
nd
Phalanx of D4 Aspect Ratio Index Wing Shape Index Tip Index
E. floridanus 67 112.5663.07 61.1361.78 21.7960.90 5.0060.45 2.8860.06 1.8460.04 63.9660.46
(adult females) 38 111.6562.92 60.4661.67 21.6060.95 5.0160.49 2.8960.07 1.8560.04 63.9860.43
(adult males) 29 113.7362.89 62.0261.54 22.0460.79 5.0060.41 2.8760.05 1.8360.03 63.9460.51
E. auripendulus . . . . 3.04 2.05 67.43
E. bonariensis . . . . 2.70 1.81 66.90
E. glaucinus . . . . 2.94 1.95 66.43
E. hansae . . . . 3.01 1.96 65.11
E. maurus . . . . 2.93 1.95 66.54
E. perotis . . . . 2.88 1.92 68.41
E. underwoodi . . . . 2.87 1.95 67.79
Dimorphism in Eumops floridanus Ober et al.
Florida Scientist 80(1) 2017 QFlorida Academy of Sciences 43
Discussion
We found modest male-biased sexual dimorphism in Eumops floridanus. Forearm
length (often used as a surrogate for overall body size in bats) was larger for males
than females, in both adults and sub-adults. In addition, two of the four measures of
wing structure were larger in adult males than females, suggesting that wings of
males are both longer and wider than those of females. The degree of difference we
observed in forearm length between sexes was 1.5%, which is similar to the degree
of sexual dimorphism found in other bat species (Williams and Findley 1979,
Lindenfors et al. 2007, Lu et al. 2014, Wu et al. 2014).
We are aware of little previous investigation into the occurrence of sexual
dimorphism in E. floridanus. Only two publications report data on forearm length
of E. floridanus. Eger (1977) describes only males and does not speculate on sexual
dimorphism. Timm and Genoways (2004) reported greater average forearm lengths
than we found, 63.9 mm for males (n¼23), and 64.7 mm for females (n¼4), and
concluded that the species was not sexually dimorphic. The differences between
our findings and those of Timm and Genoways (2004) may be because: 1) we
measured live specimens while they measured preserved museum specimens,
which can produce discrepancies (Bininda-Emonds and Russell 1994, Simmons
and Voss 2009, Stephens et al. 2015), 2) their sample size was not large enough to
accurately capture the variation in forearm length within and between sexes, and/or
Figure 2. Mean 6SE in body condition index (BCI) among Eumops floridanus of different sexes and
reproductive categories.
Ober et al. Dimorphism in Eumops floridanus
44 Florida Scientist 80(1) 2017 QFlorida Academy of Sciences
3) their small sample size resulted in analyses that lacked adequate power to detect
differences between sexes. Regardless, potential differences in measurements from
live and preserved specimens do not influence the comparisons between sexes we
report, as all our measurements were on live animals.
Sexual dimorphism is often explained by sexual selection. It has been argued
that sexual selection in males is the primary evolutionary force selecting for larger
body size (Ralls 1977, Blanckenhorn 2005). Further, it is common for males to be
slightly larger in size than females among mammal species that have a harem social
structure due in part to male - male competition (Racey 2009). There is evidence
that E. floridanus use a harem social structure (Ober et al. 2016) and our finding of
gular glands in males but not females provides additional evidence to support the
potential role of sexual selection. These glands are present in several species of
Molossids (Horst 1966, Gutierrez and Aoki 1973, Gustin and McCracken 1987,
Scully et al. 2000), and had been noted previously for Eumops in general (Eger
1977), and more specifically in E. glaucinus (Silva Taboada 1979, Bowles et al.
1990) and E. floridanus (Belwood 1992). In most species these gular glands are
well developed in males and rudimentary or lacking in females (Horst 1966, Scully
et al. 2000), as we found in the present study. In other species, these glands undergo
seasonal fluctuations in size, becoming swollen with sebaceous oils during breeding
seasons (Gutierrez and Aoki 1973, Krutzsch 2000), but understanding of their exact
function is limited. It has been proposed that these glands may be used in harem
defense and roost site marking (Belwood 1992).
Sexual size dimorphism may result in sex-specific niche utilization (Selander
1966, Williams and Findley 1979). Individuals with high wing loadings (defined as
body mass/wing area) tend to have fast flight speeds but low maneuverability
(Aldridge and Rautenbach 1987, Norberg and Rayner 1987). The larger wing size
of adult males relative to females results in lower wing loading for males, which
may slightly lessen niche overlap during the energetically demanding phase of
pregnancy. As the only species known to form harems in the U.S., niche
differentiation may be especially important for E. floridanus because individuals
are not sexually segregated during the maternity season, as is the case with the
majority of temperate species (Bradbury 1977, Senior et al. 2005). Future
investigations of whether males and females forage in different habitats or at
different distances from roosts would better inform recovery plans for the species.
The two better-known Eumops species that occur in the U.S. (E. perotis and E.
underwoodi) are considered to be among the fastest flying species in the country.
(Vaughan 1966, Findley et al. 1972). Eumops perotis and E. underwoodi are found
in dry regions at high elevation in the western U.S., Mexico, and Central and South
America where they forage in open habitat. They roost in shallow caves and
crevices in cliffs and rock walls that provide a substantial vertical drop to enable
launch into flight after roosting (Kiser 1995, Best et al. 1996), as well as in cavities
in tall plants with minimal foliage to impede the bats’ approach (i.e., royal palms
(Roystonea; Hellebuyck et al. 1985) and saguaro cacti (Carnegia gigantea; Tibbitts
et al. 2002). Our results indicate that although E. floridanus has an aspect ratio
index similar to these species, it has a lower wing shape index (the second lowest
Dimorphism in Eumops floridanus Ober et al.
Florida Scientist 80(1) 2017 QFlorida Academy of Sciences 45
among all eight Eumops species for which this has been reported), and a lower tip
index (the lowest among all species in the genus). Collectively, this suggests E.
floridanus has shorter or wider wings with shorter wing tips than most other
Eumops. While E. floridanus may not be capable of flight speeds as fast as some of
the other species in the genus, it may not need to fly as fast to generate enough lift
to remain airborne (Findley et al. 1972). When commuting through open space, E.
floridanus may incur slightly higher metabolic costs than other species in the genus,
but this may be compensated for with lower metabolic costs when maneuvering in
more confined air space (Voigt and Holderied 2012). Eumops floridanus may
encounter more clutter than other species in the genus, roosting in pines (Pinus
palustris and P. elliottii; Angell and Thompson 2016, Braun de Torrez et al. 2016)
located in pine flatwoods and scrubby flatwoods, which are more cluttered than the
desert areas typically inhabited by E. perotis and E. underwoodi. Future studies of
foraging habitat use and flight speeds of E. floridanus are recommended.
Knowledge of the ecology and physiology of E. floridanus is extremely
limited, yet is critical due to the species designation as federally endangered. The
morphological data we report serves as a foundation for our understanding of
sexual dimorphism, body condition, and flight capabilities of E. floridanus.We
found that these bats exhibit moderate sexual dimorphism in wing size, suggesting
there may be niche partitioning between sexes. Thus, we may need to consider the
foraging habitat use of males and females independently. The baseline body
condition and mass we report can be used in future studies to examine associations
between individual variation in physiological condition and environmental
conditions, habitat use, and movements.
Acknowledgments We thank the individuals who assisted with data collection, especially Ralph
Arwood, Josh Birchfield, Ryan Brown, Terry Doonan, Paula Halupa, Marilyn Knight, Jennifer Myers,
Kevin Oxenrider, Cason Pope, Jessica Reha, Frank Ridgeley, Kathleen Smith, Lisa Smith, and Seth
Sofferin. This research was funded through the Florida State Wildlife Grants Program and the Florida
Nongame Wildlife Trust Fund.
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Submitted: July 4, 2016
Accepted: August 25, 2016
Ober et al. Dimorphism in Eumops floridanus
48 Florida Scientist 80(1) 2017 QFlorida Academy of Sciences
... Males also have functional gular glands (Fig. 3), which are distinct sebaceous glands on the throat that change in appearance with reproductive status and are most obvious on large, reproductively active males . Ober et al. (2017b) recorded forearm lengths (60.0-69.1 mm) and body masses (27-59 g) for 201 E. floridanus of mixed sexes, ages, and reproductive statuses from Charlotte County. The mean mass (± SD) of 16 nonreproductive, adult males was 40.68 ± 5.79 g and for 46 nonreproductive, adult females, it was 40.47 ± 3.32 g ). ...
... The wing aspect ratio of E. floridanus likely results in lower metabolic costs while flying in cluttered habitats at slow speeds but higher metabolic costs while flying in more open areas as compared to other Eumops species . Male E. floridanus had wider wings (n = 29, x = 62.02 ± 1.54 mm) than females (n = 38, 60.46 ± 1.67 mm) and longer wings (113.73 ± 2.89 mm) than females (111.65 ± 2.92 mm- Ober et al. 2017b). However, wingtip width (combined length of the first and second phalanges of the fourth finger) did not differ between the sexes, and lengths of the first and second phalanges were similar between males and females . ...
... Surveys have been initiated within the distribution of E. floridanus to monitor known roosts and discover new roosts (FWC 2013). In addition, bat houses have been installed and monitored at sites where E. floridanus is known to occur (FWC 2013;Bailey et al. 2017a;Ober et al. 2017b). With dominant males remaining close to the roost and exhibiting roost defense, it is important to consider the foraging habitat near roosts and the distance between roosts as parameters for artificial roost placement and roost conservation (Braun de Torrez et al. 2020). ...
Article
Eumops floridanus (Allen, 1932) is a molossid commonly called the Florida bonneted bat or the Florida mastiff bat. Eumops floridanus is the largest species of bat in Florida and is one of 16 species in the genus Eumops. With one of the smallest distributions of any bat in the United States, it is endemic to southern peninsular Florida where it roosts in cavities of live and dead trees and man-made structures. Eumops floridanus was formerly classified as a subspecies of E. glaucinus but has been elevated to species level based on morphology. Due primarily to its restricted distribution, small population size, and the continued loss of habitat, E. floridanus is federally listed as “Endangered” (EN) by the United States Fish and Wildlife Service.
... Reproductive status for males was categorized as nonreproductive or reproductive through the presence of abdominal or descended testes. We calculated body condition index (mass/ forearm length) of each individual to serve as a relative measure of bat condition (Jonasson and Willis 2011, Reynolds et al. 2009) that could be compared with reports for Florida Bonneted Bats roosting in a natural area (reported in Ober et al. 2017b). ...
... The body condition indices (BCI) of bats of all sex and reproductive condition categories captured during this investigation were lower than those reported for Florida Bonneted Bats in a natural area (Ober et al. 2017b) ( Table 2). Small sample sizes precluded our ability to determine if differences were statistically significant. ...
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Florida Bonneted Bats, Eumops floridanus, were first documented in Miami, Florida, USA, in the 1930s. We summarized reports of these bats in the greater Miami area throughout the past 80 years and documented new roosts by radio-tracking bats captured in semi-natural areas. Florida Bonneted Bats in Miami consistently roosted in buildings, in contrast to other portions of the species’ range where they use trees and bat houses. Throughout the past 60 years, reports of building use have been confined to a small (40 km2) portion of the city. Bats regularly selected buildings with architectural similarities (Mediterranean Revival style; characterized by stucco exteriors, open chimneys with integrated arch covers, and clay tile roofs). To ensure adequate con- servation measures are taken to minimize harm to this federally endangered species in urban areas, we outline four topics in need of additional research and suggest four topics that should be covered through targeted educational campaigns.
... We did not find E. floridanus to be influenced by measures of flight space (total flight space or canopy flight space). As a large bat species with high wing loading and aspect ratio, they often forage above the forest canopy or open habitats and therefore are less likely to need to maneuver beneath the canopy when there are other options available (Norberg & Rayner 1987;Ober et al. 2017;Webb 2018). The tendency of this species to fly in open areas may also explain the unexpected positive association with percentage of roadway. ...
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Restoring lost or degraded wetlands is a major challenge in contemporary conservation. Understanding how wetland restoration and changes in hydrology affect wildlife is increasingly urgent for endangered species conservation. This is especially pertinent for the endangered Florida bonneted bat (Eumops floridanus), whose range is almost entirely contained within one of the world's most iconic wetland systems, the Greater Everglades Ecosystem. We investigated how E. floridanus may respond to future hydrological and vegetation changes associated with current and planned Everglades hydrologic restoration efforts. We conducted acoustic surveys at 194 random points stratified across a restoration gradient (no hydrologic restoration, partial hydrologic restoration, full hydrologic restoration, and reference). Using generalized linear mixed models, we determined the most important predictors explaining variation in bat activity and foraging likelihood. Positive associations between bat activity and several hydrologic variables expected to increase with restoration (hydroperiod, water depth, distance to canals, and extent of freshwater forested wetlands, ecologically intact reference areas, and zones with full hydrological restoration) suggest that foraging habitat for this species will likely benefit from hydrologic restoration both in the near term (immediate increases in hydroperiod and water depth) and in the longer term (as freshwater forested wetlands expand). Our results inform immediate management decisions for this species and suggest the benefits of restoration for wildlife adapted to historically longer hydroperiods and greater water depths, which are anticipated to increase with the gradual return of natural hydrological regimes.
... Geoffroy Saint-Hilaire, 1818) (Smithers 1971). Por otro lado, tomando en cuenta las medidas alares (longitud del antebrazo, y ancho y largo del ala) se ha encontrado en Eumops floridanus (G.M. Allen, 1932), que los machos son de mayor tamaño que las hembras (Ober et al. 2017). En el mismo sentido, Willig (1983), en base a seis caracteres externos y 16 craneales indicó que los machos de M. molossus son de mayor tamaño que las hembras. ...
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Se describen los patrones de uso temporal de un refugio de Nyctinomops macrotis (Gray, 1840) en el Campus de la Universidad Nacional de Piura (Perú), así como el dimorfismo sexual y los patrones reproductivos observados, desde octubre de 2017 a julio de 2018. El refugio se ubica en la grieta de un edificio, donde se obtuvieron 54 capturas (24 machos y 30 hembras). En marzo se capturó el mayor número de individuos y hembras preñadas. También se reporta la presencia de dimorfismo sexual a partir de la longitud del antebrazo. El uso de áreas urbanas como refugio de reproducción revela la importancia de estas para la fauna silvestre.
... Our results are supported by a recent study that used Global Positioning System (GPS tags to track movements of 20 Florida bonneted bats and found that males had smaller home ranges, shorter foray loop lengths and traveled shorter maximum distances from their roosts than females (Webb, 2018). Additionally, similar to Ober et al. (2017b), we found that males in all status categories had larger forearm lengths than females (and hence larger wings). It is possible that the reduced wing loading from larger wings may benefit males by conferring greater maneuverability and lower energy expenditure if they invest considerable time flying near roosts during defense. ...
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Understanding sociality and animal behavior is critical for developing effective conservation strategies. Many tropical bat species form harems, where dominant males play key social roles by defending groups of females directly (female-defense polygyny) and/or the resources that females need (resource-defense polygyny). The Florida bonneted bat (Eumops floridanus) is an endangered subtropical species suspected to form harems, but our understanding of its social structure, reproduction, and behavior is rudimentary. In this study, we evaluated demographic variation in morphological and behavioral characteristics of Florida bonneted bats to test the hypothesis that this species forms harem groups and exhibits resource-defense polygyny at roost sites. We used a 4-year dataset of 341 individuals uniquely marked with passive integrated transponders (PIT tags), coupled with tri-annual capture records, to track activity patterns of bats at five roosts fitted with PIT tag readers. We identified the likely dominant males and other demographic groups in each roost using morphometric characteristics and reproductive status. We assessed differences between sexes and among status categories in three primary metrics: amount of activity at the roost, time of emergence, and initial foray duration per night. Dominant males consistently were the most active individuals at roosts and spent the least amount of time away from roosts during forays, relative to females and other males. Females spent more time away from roosts than males and shared similar foraging activity patterns regardless of status. Our findings suggest that Florida bonneted bats form small harem groups that are active year round. Male bats exhibit characteristics of resource-defense polygyny at roost sites and a size-biased hierarchy, with the largest reproductively active males appearing to defend the roost at the expense of time spent foraging. We suggest that the roost site represents a critical, limited and defendable resource for male Florida bonneted bats to gain access to females, which has important implications for the conservation and enhancement of roost sites. Our study highlights the importance of accounting for differences in behavior across demographic groups and social roles when considering resource needs for imperiled species.
... Water levels fluctuate seasonally, with approximately 40% of the study area flooded during the summer wet season (FWC 2003). In BWWMA, Florida bonneted bats roost in cavities in pine trees and in bat houses mounted on poles across the property (FWC 2003;Ober et al. 2017). ...
Article
Full-text available
Aberrant patches of white skin or fur known as hypopigmented marks have been observed in many mammal species worldwide, but they are typically limited to only a few individuals in a population. Hypopigmented marks were documented in only two museum specimens of the federally endangered Florida bonneted bat ( Eumops floridanus) as early as 1950, but recent observations suggest that these marks may be more common in this species than previously believed. To better understand the occurrence and persistence of hypopigmented marks in Florida bonneted bats, we evaluated the variation in frequency, compared effects on survival, and assessed spatial and temporal differences of specimens at an intensively studied site and across the species range. From 2014 through 2017, we regularly captured Florida bonneted bats for demographic studies at Babcock–Webb Wildlife Management Area in Charlotte County and we observed hypopigmented marks on 172 (80.8%) of 213 individuals, the highest incidence known for bats. The proportion of hypopigmented marks did not differ with sex, age at first capture, or reproductive status, and importantly, we documented the persistence of hypopigmented marks in individuals over multiple months. We also found no difference in survival or capture probability between hypopigmented and solid-colored individuals. Using data from concurrent mist-net studies, we assessed the proportion of Florida bonneted bats with hypopigmented marks across the species range and found a higher proportion of individuals with hypopigmented marks in the two northern counties (80.8% in Charlotte County and 61.5% in Polk County) compared with the two southern counties (21.1% in Miami–Dade County and 16.7% in Collier County). Additionally, we compared the proportion of hypopigmented individuals in Miami–Dade County between recently captured/collected bats (post-2004) and historically (pre-1965) collected museum specimens and found more hypopigmented marks in recently captured bats. The persistence of hypopigmented marks over time, the presence of marks on bats from different locations, and our finding of no effect of age on the presence of marks all strongly suggest that the hypopigmented marks in Florida bonneted bats are the result of genetic rather than environmental factors. Further study is required to understand the mechanism underlying the high incidence of hypopigmented marks and to determine whether the prevalence of hypopigmented marks indicates low genetic diversity that could threaten Florida bonneted bats.
... Although it appears to use fire-dependent vegetation communities for roosting (Belwood 1992;Angell and Thompson 2015;Braun de Torrez et al. 2016) and foraging (Bailey et al. 2017;Braun de Torrez et al. 2018b), and may actually be attracted to recently burned areas (Braun de Torrez et al. 2018a), we know little about how fire regimes influence this species on a broader scale. Because Florida bonneted bats do not migrate or hibernate, and likely have an extended period of reproduction in which non-volant young are present in roosts for much of the year (Ober et al. 2017a), the habitats of these bats are exposed to fire management year round. Bats in other regions appear to tolerate or benefit from certain aspects of fire (Loeb and Waldrop 2008;Buchalski et al. 2013;Cox et al. 2016;Lacki et al. 2017;Austin et al. 2018), but we still have a limited understanding of how specific components of fire regimes, such as frequency or season of fires, influence bats over the long-term (Perry 2012). ...
Article
Full-text available
Fire suppression has altered ecological communities globally. Prescribed fire regimes strive to restore function to these fire-dependent ecosystems by mimicking natural fire regimes. Although fire frequency is a widely acknowledged component of fire regimes, the importance of fire seasonality for biodiversity is less clear but appears to play a critical role for a variety of taxa, particularly in the North American Coastal Plain. In subtropical Florida, USA, fire historically occurred primarily at the transition from the dry to wet season (early wet season: April to June) when dry fuel accumulation coincides with a high incidence of lightning. We investigated the effects of fire frequency and season on endangered Florida bonneted bats (Eumops floridanus [G.M. Allen, 1932]), a species endemic to a region that evolved with frequent fires. We surveyed bat activity acoustically in 149 sites in fire-dependent vegetation communities (pine flatwoods and prairies), and evaluated the effects of fire frequency and seasonality, using burn records from the previous 18 years. Variation in bat activity was best explained by both fire frequency and season: bat activity decreased with early wet season (April to June) burn interval and increased with dry season (November to March) burn interval. Bat activity and foraging activity were highest in sites burned at > 3- to 5-year intervals during the early wet season. Fires during the historic fire season at a moderate frequency (> 3 to 5 yr) appear to optimize habitat for bats in both pine flatwoods and prairies, likely through increases in roosts, flight space, and insect prey availability. It appears that Florida bonneted bats are fire-adapted and benefit from prescribed burn programs that closely mimic historical fire regimes. We encourage consideration of both fire frequency and seasonality when managing ecosystems with fire.
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Knowledge of the genetic structure and cryptic diversity is essential for the conservation of endangered species. We conducted a genetic survey of the federally endangered Florida bonneted bat (Eumops floridanus) sampled from its USA range in southern Florida. Florida bonneted bats are primarily found in four regions separated by approximately 100 to 250 km, including three western natural areas: Babcock Webb WMA (BW), Polk County (PC), and Collier County (CC) and one urban population on the east coast, Miami-Dade County (MD). We used 22 microsatellite loci and cytochrome b sequences to assess the extent of connectivity and levels of genetic diversity. Populations were highly differentiated at microsatellite loci (overall FST = 0.178) and model-based and ordination analyses showed that MD was the most distinct among pairwise comparisons. Regional populations were small (Ne < 100) with no evidence of inbreeding. Contemporary migration and historic gene flow suggested that regional populations have not frequently exchanged migrants, and thus the divergence among western regions was likely a result of genetic drift. Significantly, mitochondrial DNA revealed that haplotypes from MD were similar or shared with those recognized as Eumops ferox from Cuba and Jamaica, and divergent (1.5%) from the remainder of bonneted bats in Florida. Our data support the management of each of the four populations as distinct population segments, and that BW, PC and CC combined are on an independent evolutionary trajectory from bats in MD. Bonneted bats in Florida appear to harbor cryptic diversity that will require a reassessment of their taxonomy.
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Polygyny is the most common mating system in mammals, and many species form uni-male multi-female groups (UM-MF units). Polygynous systems are traditionally distinguished according to male reproductive strategies, such as “resource defense” or “female defense,” both of which are often described in the literature as forming “harems.” However, this focus on male strategies, and the use of umbrella terms to describe them, lumps together societies that fundamentally differ in their ontogeny, stability, and relationships. Integrating foundational theories of mating strategies with the principles governing relationship dynamics, driven by both male and female strategies and modulated by male-female conflicts of interest, we propose a new framework for classifying the diversity of UM-MF units. We differentiate UM-MF groups in terms of average female kinship within the group and length of male tenure to define general classes with distinct predictions for the nature of inter- and intrasexual relationships. We propose a narrower definition for the “true harem” along with new terminology to describe the other three classes: “benign consortship,” “coterie,” and “coercive consortship.” Using socioecological data for 40 mammalian species from 27 families, we found our framework was able to successfully predict patterns of female-female cooperation and the presence of coercive male-female relationships. Finally, we refine our framework, identifying subclasses of the main four classes and propose hypotheses about the underlying causes of observed patterns. By focusing on the nature of within group relationships, this framework provides a powerful lens for asking broad, comparative evolutionary questions about social evolution and socioecology.
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Knowledge of genetic structure is essential for the long-term management and conservation of endangered species. We report the results from a genetic examination of the federally endangered Florida bonneted bat ( Eumops floridanus ) sampled from its range in southern Florida, USA. Bonneted bats are primarily found in four regions separated by approximately 100 to 250 kms, including three western natural areas (BW, PC, and CC) and one urban population on the east coast [Miami-Dade County (MD)]. We used 22 microsatellite loci and cytochrome b sequences to assess the extent of connectivity and levels of genetic diversity. Regional populations were highly differentiated ( F ST = 0.178) and model-based and multivariate analyses showed that MD was the most distinct among pairwise comparisons. Regional populations are small (i.e., N e < 100) but demographically stable. Estimates of contemporary migration and historic gene flow suggest that regional populations do not frequently exchange migrants, but simulations suggest that the divergence among western regions is likely a result of recent genetic drift rather than long-term isolation. Significantly, mitochondrial DNA revealed that haplotypes from MD were similar or shared with those recognized as Eumops ferox from Cuba and Jamaica, and divergent (1.5%) from the remainder of bonneted bats in Florida. Our data support the management of each of the four populations as distinct population segments, and that BW, PC and CC combined are on an independent evolutionary trajectory from bats in MD. Critically, bonneted bats in Florida appear to harbor cryptic diversity that will require a reassessment of their taxonomy.
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Effective strategies for bat conservation require knowledge of species-specific roost ecology. Thus, conservation planning is difficult for species with poorly understood roost use, such as the federally endangered Eumops floridanus (Florida Bonneted Bat). Prior to this study, only 1 active natural roost had been documented throughout the Florida Bonneted Bat's geographic range. Search efforts to locate new roosts using several techniques have been unsuccessful. Here we present a simple methodology that we successfully implemented to locate a second Florida Bonneted Bat natural roost. Using acoustics, cavity searches, and emergence observations, we documented a colony of Florida Bonneted Bats roosting in a Pinus elliottii (Slash Pine) snag in Florida Panther National Wildlife Refuge in Collier County, FL. Our discovery highlights the importance of snags, and provides additional details to state and federal agencies tasked with species recovery.
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Body size is arguably the most important morphological trait of animals. Males and females' body size differences as sexual size dimorphism (SSD) affect behavioural and ecological processes. We study sexual size dimorphism in small mammals, collecting 95 species (22 Chiroptera, 66 Rodentia, 1 Scandentia, and 6 Soricomorpha) from published literatures. The sexual difference in size between the sexes is not-significant either in 33 little female-biased SSD or in 62 little male-biased SSD species. The non-significant difference in body size of 62 little male-biased SSD species showed that sexual selection did not drive the evolution of male body size, with weaker correlated selection on female body size. Data analysis revealed a non-significant correlation between female body length and litter size in 33 species, suggesting that fecundity selection in favour of larger females is unlikely to play a role for explaining SSD lacking in small mammals.
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For bats, when secondary sexual dimorphism is significant, females typically are larger than males. Moreover, in mammals, variation in the degree of sexual dimorphism often follows an allometric relationship whereby differences vary with body size (Rensch's rule). We examined sexual dimorphism across the New World clade of Myotis regarding species-specific and clade-wide patterns of body, cranium, and wing size, Rensch's rule and degree to which such morphological variation is related to phylogeny. Size differences were common with significant cases of both male-biased and female-biased sexual dimorphism. In more than half the cases, females were larger than males. Variation in degree of dimorphism exhibited an allometric pattern. Nonetheless, slope of the relationship between size and degree of dimorphism was no different from unity (i.e., isometry), failing to support Rensch's rule. There was a strong and significant relationship between phylogeny and morphological variation but not between phylogeny and degree of dimorphism. Patterns suggest that differences between males and females enhance aerodynamic capabilities of females whereby larger mothers can overcome constraints on flight due to the mass of large fetuses and newborns.
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The use of standard external measurements is pervasive in mammalogy, due in part to their applicability to both living and dead animals. Nevertheless, comparisons of measurements made between animals in different pre- and postmortem body states may be problematic. To investigate the impact of body state on standard measurements and their associated variances, we took 5 external measurements on 70 Mus musculus while living and in 3 postmortem body states (primary flaccidity, rigor mortis, and secondary flaccidity). Total length, tail length, and hind-foot length were significantly longer in states of primary and secondary flaccidity than when measured on live individuals or those in rigor mortis. Ear length increased from living to primary flaccidity, after which it decreased. Weight decreased between each postmortem body state, likely as an artifact of desiccation. Variance was always greater for measurements taken in the living state than during postmortem body states. Irrespective of body state, variance was particularly high for ear length and hind-foot length, which are prone to observer bias and should be used with caution. Additional tests using field-collected data from populations of Peromyscus leucopus and Peromyscus maniculatus confirmed our lab-based results from M. musculus. External measurements taken during a postmortem state should not be compared to measurements from live animals and could lead to incorrect species identification. Additionally, comparisons among individuals measured in different postmortem body states may confound efforts to assess changes in body size over space or time.
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Guidelines for use of wild mammal species are updated from the American Society of Mammalogists (ASM) 2007 publication. These revised guidelines cover current professional techniques and regulations involving mammals used in research and teaching. They incorporate additional resources, summaries of procedures, and reporting requirements not contained in earlier publications. Included are details on marking, housing, trapping, and collecting mammals. It is recommended that institutional animal care and use committees (IACUCs), regulatory agencies, and investigators use these guidelines as a resource for protocols involving wild mammals. These guidelines were prepared and approved by the ASM, working with experienced professional veterinarians and IACUCs, whose collective expertise provides a broad and comprehensive understanding of the biology of nondomesticated mammals in their natural environments. The most current version of these guidelines and any subsequent modifications are available at the ASM Animal Care and Use Committee page of the ASM Web site (http://mammalsociety.org/committees/index.asp).
Article
Many Chiropteran species are gregarious, yet much remains to be learned about details of the sociality of most species. This is especially true for the endangered Eumops floridanus (Florida bonneted bat). Scant knowledge of the species’ natural history and ecological interactions has precluded the development of effective conservation strategies. We investigated several aspects of the social organization of E. floridanus roosting in bat houses in southwest Florida: group size, group composition, group stability, and seasonality of reproduction. Our findings suggest the species has characteristics more common to tropical bat species than temperate ones. The average roost size was 10 individuals, with colonies in a harem social structure all three times in the year they were assessed. Adults were much more likely than sub-adults to be recaptured at the same roosts during subsequent capture sessions. We suggest that the availability and distribution of roosts may alter the social structure of these bats and ultimately limit local populations. We did not find evidence of a distinct seasonal birthing period matching that of other temperate bat species. Results suggests the species is aseasonally polyestrous, making non-volant E. floridanus vulnerable to disturbance across a larger portion of the year than other bat species in the US.
Chapter
Introduction and MotivationSelf-organization in Today's InternetSelf-organization in Ad Hoc and Sensor NetworksSelf-organization in Network ManagementGraph-theoretical Aspects of Self-organizationPotential and Limitations of Self-organizationAcknowledgementReferences
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This chapter reviews the current knowledge about the biology of male reproduction in Chiroptera. Special attention is given to the functional cyclicity and gross and microscopic morphology of the primary, accessory, and secondary sexual structures of the male reproductive tract. The general morphological plan of the organs that it comprises is relatively conservative in gross and microscopic structure. There is, however, variation in the complement and appearance of organs within and between taxonomic groups. Male bats also exhibit diversity in the timing and frequency of their reproductive cycles annually; in some species this may be expressed in a unique functional (dysynchronous) timing between primary (testes) and accessory (prostate, ampullary, seminal vesicles, urethral and Cowper's) sex glands. Permissive to this pattern can be the prolonged retention of viable spermatozoa in the caudae epididymidides and extended accessory sex gland function to effect additional intermittent winter mating by males who apparently retain their libido beyond the fall copulatory period. There are many gaps in the basic knowledge of the morphology and physiology of the male reproductive system of Chiroptera. Only a few taxa have been examined over an extended period of time (one or more annual cycles) in which seasonal changes in the system have been recorded and related to organ structure and physiological function.
Article
A method was devised for estimating aspect ratio, wing ratio, wing area, wing loading, and wing length from study skins of bats. These measures were taken of 136 species representing 15 families. Wing area and loading are positively, and wing length negatively, correlated with size. Aspect and tip ratios are independent of size and of each other. Distinctive combinations of some of these variables characterize groups of bats that presumably have similar flight modes. Speed is positively correlated with aspect ratio and tip index, but regresses significantly only on the former. Long tips coupled with low aspect ratio may characterize hoverers. Long wings and short tips may characterize bats that are capable of remaining airborne at slow speeds. Most bats with low aspect ratios are forest dwellers, whereas species with high aspect ratios are migrants and foragers in open areas.
Article
Of the six species of free-tailed bats from selected sites in northwestern Yucatan, Molossus sinaloae was taken most frequently, followed in order by Eumops glaucinus, Molossus ater, Eumops bonariensis, Promops centralis, and Tadarida laticaudata. Tile roof roost data for M. ater, M. sinaloae, and E. bonariensis showed some aggregation and, for the latter two, some roost fidelity.