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USE OF A GELATIN SUSPENSION METHOD TO EXAMINE LACK OF SEXUAL DIMORPHISM IN CRANIAL CAPACITY OF TADARIDA BRASILIENSIS FROM OKLAHOMA.

Mammalian sexual dimorphism has been described as males being larger than females in body size or possessing secondary sexual characteristics that females lack (Ralls, 1977). However, for some bat species, reverse sexual dimorphism (females being larger than males) has been documented (Ralls, 1976; Myers, 1978; Ascorra et al., 1991; Lison et al., 2014). In Brazilian free-tailed bats, Tadarida brasiliensis, sexual dimorphism exists in dental features (Herreid, 1959), the pelvic skeleton (Crelin and Newton, 1969), and some wing measurements and body mass (Lowery, 1974; Hunter, 2001), although there is no physical difference in pelage feature (Nason, 1948). Comparisons of the cranial capacity of male and female Tadarida have not been made. The purpose of this study was to determine if any differences exists in cranial capacity and cranial dimensions of male and female Brazilian free-tailed bats from western Oklahoma. We also describe a method of injecting a gelatin suspension into the cranial cavity to estimate volume of each skull.

Cranial volumes were estimated for 128 adult T brasiliensis skulls (47 males; 81 females). The skulls were from bats collected in north central Oklahoma and are deposited in the University of Central Oklahoma Natural History Museum and Oklahoma State University Collection of Vertebrates. using bats from a restricted geographic region allowed for examination of sexual dimorphism in a particular area and reduced the possibility of geographic variation (Myers, 1978).

We injected a gelatin (Knox Gelatin, Kraft Foods Group Inc., Northfield, Illinois) suspension into the cranial cavity to estimate volume of each skull (N = 128). The gelatin was softened in 59 mL of room temperature water and then 177 mL of boiling distilled water was added to the water-gelatin suspension and stirred until the gelatin dissolved. One-milliliter syringes (0.10 cc subdivisions; Duda Energy Industrial LLC., Decatur, Alabama) were filled with the gelatin suspension and allowed to congeal in a refrigerator (1.6[degrees]C) for 4 h. We injected the gelatin suspension through the foramen magnum into the cranial cavity until it was filled. We estimated the amount injected to the nearest 0.01 cc. To remove the gelatin, we injected warm water (50[degrees]C) into each cranium with a syringe fitted with a blunt tip needle. The skulls were dried in a laboratory oven at 95[degrees]C.

Cranium measurements were made with a digital caliper (0.01 mm; Neiko Tools USA, China). The greatest length of skull (GLS) was measured from the most anterior part of the center of the premaxillary bone to the most posterior point of the occipital bone. Length of braincase (LBC) was measured from the posterior point of the postorbital process to the most posterior point of the occipital bone. Breadth of braincase (BBC) was the greatest width across the braincase posterior to the zygomatic arches. Height of skull/braincase (HBC) was measured using the depth gauge of the digital caliper. The skull was placed on a glass microscope slide and the depth determined along a vertical axis from the top of the glass to the highest point on the partial bone to the lowest point of the auditory bullae. An external/outer estimate of the volume of the cranium (OCV) was estimated by multiplying the LBC x BBC x HBC.

Two individuals, working independently, estimated the cranial capacity volume and recorded cranial measurements for each skull. Differences between the measurements made by the individuals were calculated and descriptive statistics were used to detect any outliers. The outliers were removed prior to determining if any significant difference existed between males and females.

Descriptive statistics (mean, standard deviation, and range) were calculated for all measurements for all individuals combined and for males and females separately. The Anderson-Darling normality test was used to examine the male and female data sets for normality, and a two-sample F-test was used to determine if the samples had equal variances ([alpha] = 0.05). Although the male and female data sets met the two main assumptions (equal variances and normally distributed data) for conducting a t-test to determine if the means were significantly different, the sample sizes were quite different (47 males, 81 females). Therefore, the Mann-Whitney test was used to determine if the male and female measurements were significantly different ([alpha] = 0.05). Because the sample sizes were large, the significance of the Mann-Whitney test was determined by employing a normal approximation (Z values) of a two-tailed Mann-Whitney test (Zar, 2010).

Table 1 contains the descriptive statistics and results of the Mann-Whitney test and normal approximations for differences in cranial measurements and cranial capacities between male and female T. brasiliensis. The mean cranial capacity volume for males was 0.205 cc, ranging from 0.158-0.238 cc. The mean cranial capacity volume for females was 0.202 cc, ranging from 0.160-0.243 cc. There was no significant difference in the cranial capacities between males and females. Combined, male and female cranial capacity volumes averaged 0.203 cc, ranging from 0.158-0.243 cc. There were also no significant differences between male and female cranial measurements or the external estimate of cranial volume. The Mann-Whitney and normal approximation Z values for GSL and LBC were the same and which was expected because the LBC is a dimensional component of the GSL and the sum of the rankings used in the Mann-Whitney tests would be the same.

In this study, we used a new gelatin suspension method to estimate the cranial capacity of small bat skulls and determine if the cranial volumes of male and female T. brasiliensis were significantly different. Previous methods have been used to estimate the volume of small skulls including filling the cranial cavity of bats with small lead shot (Findley 1969), filling the skull with small mustard seeds, or imaging methods (Manjunath, 2002). Our use of a gelatin suspension eliminates variation due to the packing of shots or seeds, is less expensive than imaging techniques, and maintains the integrity of the skulls.

The lack of significant differences in the cranial volumes or other cranial measurements of T. brasiliensis skulls from bats in western Oklahoma agrees with Myers's (1978) suggestion that there is less dimorphism in bat heads and tails due to the need for weight reduction at the anterior and posterior ends of the body for flight. Myers (1978) also suggested that dimorphisms in bats might be the result of competition for a limited dietary resource or that female size differs because of the need to effectively fly while carrying a growing fetus, producing and carrying milk to nourish the young, or carrying the young post birth. Wilkins (1989) stated that if the sexes have similar diets and the females do not routinely carry young while flying, there might be reduced dimorphism. Females of the genus Tadarida do not carry their young while foraging, and young are left each evening in creches in the maternity caves (Caire et al., 1989; Wilkins, 1989). The few food habit studies that have been conducted on T. brasiliensis (Ross, 1961, 1967; McWilliams, 2002, 2005; Lee and McCracken, 2005) have not included bats from western Oklahoma, and few have examined if differences exist in the diets of males and females. McWilliams (2002) reported there was not a difference in the diets of males and females during the summer season at Carlsbad Caverns except in June during late pregnancy and early lactation. Kunz et al. (1995) reported there was no significant difference in the diets of pregnant and lactating T. brasiliensis. Lepidopterans and coleopterans were documented as the primary dietary components (Kunz et al., 1995). It is interesting to note that Brazilian free-tailed bats have a very high milk fat content (28%), allowing for rapid development of offspring (Wilkins, 1989; Kunz and Robson, 1995; Gannon et al., 2005).

Most males do not return to the maternity areas in Oklahoma (Glass, 1982; Caire et al, 1989), which reduces competition for food resources between the sexes and causes less pressure for selection of dimorphism in cranial measurements to handle different prey items. Body and wing features and dimensions of male and female T. brasiliensis from western Oklahoma have not been examined but might show dimorphisms due to need of the female to effectively fly and carry the fetus prior to birth and lactation post birth. It might be interesting to compare cranial capacities and other morphological features of males and females across the distributional range of T. brasiliensis to determine if regional differences exist and if ecological selective pressures influence dimorphisms. Ecological and economic values of free-tailed colonies have been well documented and therefore warrant further investigation of this species.

We thank K. McBee and J. J. Lovett at the Oklahoma State University Vertebrate Collection for the loan of specimens. N. Nieves at the University of Central Oklahoma provided the Spanish translation of the abstract. We also thank the University of Central Oklahoma laboratory manager, W. Unsell, for assistance with equipment and supplies.

Literature Cited

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Submitted 10 July 2016. Accepted 1 April 2017.

Associate Editor was Roger Rodriguez.

William Caire, * Miranda J. Gilbert, Mackenzie A. Endebrock, and Lynda Samanie Loucks

Department of Biology, University of Central Oklahoma, Edmond, OK 73034

* Correspondent: wcaire@uco.edu
Table 1--Descriptive statistics for cranial measurements (a) and
cranial capacities (b) of male and female Tadarida brasiliensis from
Oklahoma. SD = standard deviation, GLS = greatest length of skull,
LBC = length of braincase, BBC = breadth of braincase, HBC = height
of braincase, CCV = cranial capacity volume, OCV = estimate of outer
cranial volume. None were significantly different (P < 0.05) based
on the normal approximation to a two-tailed Mann-Whitney test.

      All (N = 128)           Males (n = 47)

      Mean     SD     Range   Mean     SD     Range

GLS   16.56   0.60    6.18    16.60   0.35    1.605
LBC   8.33    0.25    1.41    8.33    0.26    1.24
BBC   8.75    0.20    1.66    8.73    0.24    1.66
HBC   7.02    0.41    2.92    7.04    0.35    1.57
CCV   0.203   0.017   0.085   0.204   0.017   0.080
OCV   0.51    0.04    0.26    0.51    0.03    0.14

      Females (n = 81)

                                           Normal
                               Mann-    approximation   Probability
      Mean     SD     Range   Whitney     Z values        values

GLS   16.53   0.71    6.18     1863        -0.195          0.845
LBC   8.33    0.25    1.40     1863        -0.195          0.845
BBC   8.76    0.17    0.72     1690         1.050          0.293
HBC   7.00    0.45    2.92     1711        -0.949          0.343
CCV   0.202   0.017   0.083    1657        -1.216          0.216
OCV   0.51    0.04    0.26     1784        -0.586          0.556

(a) All cranial dimension measurements are in millimeters.

(b) All cranial capacity volumes are in cubic centimeters.
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Title Annotation:Notes
Author:Caire, William; Gilbert, Miranda J.; Endebrock, Mackenzie A.; Loucks, Lynda Samanie
Publication:Southwestern Naturalist
Geographic Code:1U7OK
Date:Jun 1, 2017
Words:2268
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