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January 2002
Call parameters and facial features in bats: a surprising failure of form following function
Amanda Goudy-Trainor University of Nebraska State Museum
Patricia W. Freeman University of Nebraska-Lincoln, [email protected]
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Goudy-Trainor, Amanda and Freeman, Patricia W., "Call parameters and facial features in bats: a surprising failure of form following function" (2002). Papers in Natural Resources. 18. https://digitalcommons.unl.edu/natrespapers/18
This Article is brought to you for free and open access by the Natural Resources, School of at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Papers in Natural Resources by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Acta Chiropterologica, 4(1): 1-16,2002 PL ISSN 1508- 1109 O Museum and Institute of Zoology PAS
Call parameters and facial features in bats: a surprising failure of form following function
AMANDAGOUDY-TRAIN OR^, and PATRICIAW. FREEMAN],
U~ziversityof Nebraska State Museum and School of Biological Sciences, W436 Nebraska Hall, U~ziversityof Nebraska-Lincolrz,z Lincoln, NE 68588-0514, USA 2~re.sentaddress: Wisco~zsirzNational Primate Research Center; 1223 Capitol Court, University of Wiscoruin, Madison, WI 53715-1299, USA 3Correspondiing author: E-mail: pfreemanl @unl.edu
We attempted to correlate echolocation call parameters to a comprehensive array of ear and nose measurements from 12 families of bats. Surprisingly, we failed to find any significant relationships. We did find consistent differences between nasal and oral emitters such as: (a) nasal emitters have higher frequencies with maximum energy for their size than oral emitters, (b) nasal emitting bats tend to have longer, narrower skulls, and (c) nasal emitters have a shorter distance from the nostril to the eye (muzzle length).
Key words: Chiroptera, call parameters, ecliolocation, nasal and oral sound emission, facial features, noseleaves, ems, muzzle length
Across and among some families, fre- quencies used by bats in echolocation calls Griffin (1958) first quantified echoloca- have been shown to be negatively correlat- tion in an aerial-hawking insectivorous bat ed with size of bat that has been derived and divided the capture sequence of signals from a variety of indicators including skull into three phases: search, approach, and measurements, forearm length, and body feeding buzz. Identification of bats by mass (Heller and Helversen, 1989; Basclay search phase calls in the field using ultra- and Brigham, 1991; Vaughan et al., 1997; sonic detectors is now common. The mix- Fenton et al., 1998; Bogdanowicz et al., ture of the constant frequency and fi-equen- 1999; Jones, 1999). Average body mass for cy liiodulation in calls, frequency change a species is not often uniformly available. over time, hamonic structure, duration, Most animals produce sounds with wave- highest and lowest frequency, and frequen- lengths equal to or smaller than their body cy with maximum energy are standard pa- size (Jones, 1999). This relationship be- tween size and sound production has special rameters monitored for identification pur- I I poses (Fenton and Bell, 1979, 1981; Thom- significance for echolocating bats because as et al., 1987; Fenton, 1994; O'Farrell et size of bat may be constrained by the fre- al., 1999). However, some species of bats quencies needed to detect prey (Barclay and cannot be differentiated by these parame- Brigham, 1991; Fenton et al., 1998; Jones, ters. 2 A. Goudy-Trainor and P. W. Freeman 1
Facial structures of bats are highly vari- frequency sounds have significantly differ- able and can include noseleaves; wart-like ently shaped ears than those emitting lower projections; papillae and slits; differing frequencies. Except for the relationships I sizes, shapes and placement of pinnae; and between size and frequency, we had no spe- various pinnae accessories such as a tragus, cific a priori predictions about relationships ? r~iltitragus and transverse ridges (Fig. 1). of facial features and echolocation strate- i Noseleaves are found in the Rhinopornati- gies. To this end we measured a wide assay dae, Rhinolophidae, Hipposideridae, Nycte- of facial features in search of possible cor- ridae, Megademalidae, Phyllostomidae and relations. in two genera of the Vespertilionidae. The first six fainilies in this list ase nasal emit- MATERIALSAND METI-IODS lers, while all other families of microchi- roplesans are 01x1 emitters (Pedersen, 1993). Sixty-six fluid-preserved specimens of species witli available ecliolocation data from 12 hmilies Oral-emitting bats can have wrinkled, thick- were obtained from the America11 Museum of Natural ened lips, lips with papillae, lip pads or History and measured (Table 1). The families repre- cornbinations of these and other facial sent a broad range of hcial fcaturcs and ecliolocation foliage. The noseleaf in nasal emitting bats calls within Chiroptera. Individual specimens were in and the mouth FIG;. 1. Facial features of nasal and oral emitting microchiropterans. (A) Trcrchops cirrlzosirs, (C)Hippo,sidrro,s ctrJ'er, and (E) Carollia persl~icillczta are nasal emitting bats, and (B) Myotis rnyotis and (D) Trrokrr-id~r negyptiaca are oral emitting bats. Drawings in A-D are adapted from Altringham (1996), E - from Husson (1962), and names of structures from Hill and Smith (1984). Measurements illustrated here and detailed in Materials and Methods are: (a) length of head; (b) width of head; (c) greatest height of head; (d) width of eye; (e) distance between eyes; (f) distance from nostril to eye; (g) distance from ear to eye; (11) least distance between nostrils; (i) distance from nostril to ear; Cj) pinna length; (k) pinna width; (1) length of tragus; (111) width of tragus; (11) length of anti-tragus; (0) width of anti-tragus; (p) distance bctwecn meatuses; (cl) brcncltl~:\cross pinnae; (r) distance between pinnae; (s) number of ridges on pinna; (1) spacing or ridges; (u) angle (31" pinna to head; (v) total length of nose leaf; (w) I~orseshoelength; (x) width of horseshoe; (y) spear or lancct Icngtli; (2) spear or lance[ width 4 A. Goudy-Trainor and P. W. Freeman TABLE1. Species, characteristics of echolocation calls and their sources, and emission types of bats in this study -- - -- Frequency Hlghest Lowest with Max, Emission GenusiSpecies D""t'on Frequency Frequency Reference Source ------.------Rhinopomatidae Habersetzer, 198 1 Nasal Simmons cr al., 1984 Mosia nigrescens 1.1 Grintiell and Hagiwara, 1972 Oral Saccopteryx bilitleafa 3.5-15 Griffin and Novick, 1955 Oral 5.9 Barclay, 1983 5.4-9.4 O'Farrell and Miller, 1997 8 Pye, 1966b 9.0-9.4 Kalko, 1995 Taphozous tnaliritianus 16 Fenton et al., 1980 20 Alclridge and Rautenbach, 1987 2.4-18 Taylor, 1999 Nycteridae Nycteris nzacrotis 0.6 57.3 84.0 Fenton and Fullard, 1979 Nilsal N,thebaica 61 Fenton, 1985 Nasal 2.0 6 1 94 Fenton and Bell, 1981 2 6 1 Aldridge and Rautenbnch, 1987 1.5-2 20.4-61 21.8-94 Taylor, 1999 Megadermatidae Megcldenna lyra 4.0 40 Leippert, 1994 0.4-1.2 Fiedler, 1979 1.o Madtnuthu efnl., 1995 1.1 Novick, 1958 Schmidt el ctl., 2000 Novick. 1958 Rhinolophidae 64 83 Jones and Rayner, 1989 69.3 82.3 Vaughan el [I/., 1997 67-63 Trappe and Schnitzlcr, 1982 70-75.2 Vogler and Neuweiler, I983 60-65 Pye, 19660 66-7 1 Roberts, 1972 42-47 Sulhers et rrl., 1988 29 Fenton 1985 29 46 Pentotl ant1 Bell, 198 1 24 Aldriclge and Raulenbach. 1087 24-29 37-46 Taylor, I999 56-58 Schnitzler et ctl., 1985 Nasal 65 Neuweiler et crl., 1987 57-60 Novick 1958 64 Fenton, 1985 Nasal 64 78 Taylor, 1999 64 78 Fenton and Bell, 198 1 Hipposideridae Hipposideros bicolor Jones et al., 1994 5-7 Novick, 1958 131, 142 Lara et ctl., 2001 Pye, 1972 ------Nnsnl Call parameters and facial features in bats 5 TABLE1. Continued ------pp -- Frequency Highest Lowest with Max. Duration Emission Frequency Frequency Energy Reference (ms> Source (Hz) (kHz) (Hz) 140 119.3 Fenton, 1986 128-153 Jones et al., 1993 140 Fenton and Thomas, 1980 137 99-1 17 Roberts, 1972 138 105 Aldridge and Rautenbach, 1987 138-145.4 105-131 138-143.5 Taylor, 1999 55-56 Pye, 1972 Nasal 62 5 1 Fenton, 1985 62 55 6 1 Fenton and Bell, 1981 65-69 50-58 Roberts, 1972 62 55 Aldridge and Rautenbach, 1987 62 55 61 Taylor, 1999 54.9 50.9 54.9 Fenton, 1982 Nasal 62 48-54 Roberts, 1972 58 47 Grinnell and Nagiwara, 1972 H. lankadiva 74 69 Novick, 1958 Nasal H. speoris 136-139 Jones et al., 1994 Nasal 120 110 Novick, 1958 125.7-134 Pavey et al., 2001 Noctilionidae Noctillo labialis 70 40 Suthers and Fattu, 1973 Oral N. leporinzrs 58-61 30-36 Suthers, 1965 Oral 52-60 27-34 Schnitzler et al., 1994 3444 23-31 Griffin and Novick, 1955 60 Pye, 1966a 60 30 Suthers, 1967 Mormoopidae Pteronot~tsdavyi 68.1 58 O'Farrell and Miller, 1997 Oral 78 63 Novick, 1963 68 Ibiiiez et al., 1999 R parnellii 64 56 Novick, 1963 Oral Griffin and Novick, 1955 50 38 Pye, 1967 60 45 6045 Pollak and Henson, 1973 63.5 54.5 O'Farrell and Miller, 1997 60.5-61.5 45-48 Roberts, 1972 P. personatrts 63 59 Novick, 1965 Oral 33 Griffin and Novick, 1955 Phyllostomidae Carollia perspicillata 76-92 70 Griffin and Novick, 1955 Nasal 80 55 Pye, 1967 Centlrrio senex 115 70 Pye, 1967 Nasal Desrnodus rotrmdrts Novick, 1963 Nasal 75-60 Griffin and Novick, 1955 75 48 Pye, 1967 Macrotus waterhortsii 78 54 Novick, 1963 Nasal Phyllostotnus hastatus 42-55 Griffin and Novick, 1955 Nasal 42-50 25-30 Pye, 1967 Trachops cirrhosus 79 53 Barclay et al., 198 1 Nasal Varnpyrrrn! spectnrtn 95-100 65 Bradbury, 1992 Nasal -- 6 A. Goudy-Trainor 'and P. W.Freeman TABLE1. Continued Frequency Highest Lowest Duration with Max. Emission GenusISpecies Frequency Frequency Reference (ms) Energy Source (kHz) (kHz) - - - .------Vespertilionidae 49 26 30 Fenton and Bell, 198 1 Oral 55 30 40-45 Fuzessery et ol., 1993 60 34 Griffin. 1958 Thomas et nl., 1987 Oral Fenton and Thomas, 1980 Oral Fenton and Bell, 1981 Aldridge and Rautenbach, 1987 Taylor, 1999 Miller and Degn, 1981 Troest and Mohl, 1986 57.4 27.7 Vaughan et al., 1997 Oral I 46 25 Barclay, 1986 Oral 30 28 Thomas et ol., 1987 41 27 Fenton et al., 1983 65 30 Barclay, 1984 37 25 Belwood and Fullard, 1984 Oral 20 17 Barclay, 1986 30 20 Fenton er ol., 1983 39 26 Fenton and Bell, 198 1 I 32 20 Barclay, 1984 80 3 1 Jones and Rayner, 199 1 Ornl I 60 40 Thonipson and Fenton, 1982 40 Thomas er rrl., 1987 Om1 60 40 Fenton et ol., 1983 67 37 Petiton and Bell, 198 1 82 40 knlon and Bell, 1979 79 33 Jones and Rayner, 1988 Oral 95 3 5 Miller 2nd Degn, 1981 90-95 25.5 Kalko and Schnitzler, 1989 81.4 29.4 Vaughan et ol., I997 7 1 37 Faure and Bat clay, 1994 Oral 40 Thotuns et a/., 1987 105 40 Fenton el ol., 1983 97 54 Fenton ancl Bell, 198 1 71.22 37 Faure er al., I990 40 Thomas et a/., 1987 Oral 62 41 Fenton el crl., 1983 78 38 Fentoil and Bell, 1981 78 40 Fenton and Bell, 1979 79.2 33.5 Herd and Fenton, 1983 85 42 Bxclay, 1984 93.2 39.6 Fenton and Fullard, 1979 78 39 GriKin, 1958 LOO 40 Ilabersetzer and Vogler, 1983 Oral 80.3 32.5 Vaughan et ol., I997 Or:~l 75 4 1 - - , I981 Oral Call parameters and facial features in bats TABLE1. Continued Frequency Highest Lowest with Max. Emission GenuslSpecies Duration Frequency Frequency Reference Energy Source 31 34 Fenton and Bell, 1981 Oral 20 Suthers, 1967 Oral 20 Griffin, 1958 35 Tliomas et nl., 1987 Oral 30 Fenton et nl., 1983 40 46 Fenton and Bell, 1981 42 46 Fenton and Bell, 1979 53 62 Fenton and Bell, 1981 Oral 60 Fenton and Thomas, 1980 Oral 62 70 Fenton and Bell, 1981 75.4 82.2 Fenton and Fullard, 1979 62 Aldridge and Rautenbacli, 1987 42.4-67.4 43.4-71.1 Taylor, 1999 f? pipistrellrrs 50 Miller and Degn, 1981 Oral sensu lato 43 Waters and Jones, 1995 45 Pye, 1966b 55 100-60 Surlykke and Miller, 1985 l? nreppelli 40 45 Fenton and Bell, 1981 Oral 40 Aldridge and Rautenbach, 1981 Scotophil~lsnigritn 28 Fenton, 1985 Oral 28 30 Fenton and Bell, 1981 Molossidae Cl7nerephon nnsorgei 16 Fenton, 1985 Oral 16 17.8 Fenton and Bell, 1981 16 18 Taylor, 1999 25-30 Pye, 1966b Oral 17 21 Fenton and Bell, 1981 Oral 40 Simmons et nl., 1978 10 13 Fenton, 1985 Oral 10-24.9 13-26.0 Taylor, 1999 10 10 Fenton and Bell. 1981 15 18 Fenton and Bell, 1981 Oral 15-18.7 18-20 Taylor, 1999 - --..- --. medial edges of nostrils; (i) distance froln notch of edges of left and right free standing pinnae; (s) num- pinna to lateral edge of nostril on the same side; 6) ber of raised transverse ridges present on inner curve pinna length from notch to tip of pinna; (k) greatest of pinna; (t) spacing of ridges is the distance averaged width across pinna either laid out on a flat surface or, fro111 3 inter-ridge measurements between ridges on if curvature is too great, folded at the curvature with inner curve of pinna; (11) angle of pinna to head taken the two separate widths added together; (1) length of on lateral side of head with protractor aligned with tragus from inferior margin at the traguslpinna junc- anterior ventral margin of the mandible, centered at ture perpendicular to tip; (m) greatest width of tragus notch of pinna and follows line of free-standing pinna and perpendicular to length; (n) length of anti-tragus through the tip; (v) total length of noseleaf from ven- from inferior margin at the anti-traguslpinna juncture tral surface of the continuous horseshoe to dorsal tip perpendicular to tip; (0) greatest width of anti-tragus of spear or lancet; (w) horseshoe length Cro~nventral perpendicular to length; (p) distance between meatus- surface of the continuous horseshoe to the continuous es from left to right external auditory canals; (q) dorsal top of horseshoe; (x) greatest width of horse- breadth across outermost edges of left and right free shoe and perpendicular to length; (y) spear or lancet standing pinnae; (r) distance between innermost length from base, near an imaginary line between 8 A. Goudy-Trainor and P. W. Freeman the two nostrils, to tip; (2) greatest spear or lancet ship between facial features and call param- width and perpendicular to length. eters. We documented from the literature the following The relationship between frequency search call parameters: duration, highest and lowest with maximum energy and the composite frequency, and frequency with maximum energy (Table 1). When two sources for a species' search call size character is significantly different were located, we averaged the search calls togelher. between nasal and oral emitting bats. Nasal When three or more search call sources were located, emitting bats have higher frequencies with we compared the calls for consistency and extreme maximum energy for their head volume values were discarded before the call data were aver- aged. Recordings we used span the 45-year history of (SIZE) than oral emitting bats as seen in echolocation data, and we took recording differences their different slopes (Fig. 2A). Overall, into account when the available call data was aver- bats with higher frequencies with maximum aged. In addition, we noted emission source Tor each energy have smaller head volumes. Al- family (Pedersen, 1993). though not significant, nasal emitting bats We used bivariate plots and regression analysis (STATVIEW) to detect patterns within our data and in this study tend to have longer, narrower compared regression Iines with Student's t-test. As in heads (below the line) than oral emitting Freeman (1984, 1988) we used the sum of the natural bats (above the line; Fig. 2B). Tlxee nasal logs of length, width, and height of head to cslinlatc emitting phyllostomids (Sphaeroizycteris head volume and thus, size of bat. Natural logs of all toxoplzyllunz, Centurio senex, Phyllostom~is but one (angle of pinna) facial measurements were regressed against this cotnposite size character (SIZE) hustatus) are exceptions. The relationship to determine whether facial measurements were cor- between the distance from nostril to eye, related. Duration is not correlated with SIZE. Wc which we designate as muzzle length, ver- regressed the measurements of facial features and sus head length is significantly different duration directly. Since all frequency parameters are between oral and nasal emitting bats such I correlated with SIZE, we calculated the residuals I from these regressions ant1 regressed the residuals that nasal emitting bats have longer overall against the measurements of racial features. Because head lengths but shol-ter muzzle lengths we made n~ultiplecomparisons of these emission (Fig. 2C). parameters to our measurements of facial features, the Most of the facial characteristics we P-value used for statistical significance has lo be measured ase significantly (P < 0.05) corre- reduced from 0.05 to 0.0005 based on the fortnula, 0.95 = (1 - a)", where II = 104 and is the numbcr of lated with SIZE. Facial features not corre- regressions run. lated with SIZE are: greatest width of anti- tragus, number of trai~sverseridges on the pinna, spacing of ridges on the pinna, angle of pinna to head, horseshoe length, and Our attempts to find significant correla- spear length. Because of strong correlations tions between our measurements of facial between most facial measurenlents and features and call parameters were weak to SIZE and the different correlations between unsatisfactory once the factor of size was frequency with inaxilnum energy versus accounted for. At this stringent value of a = SIZE for nasal and oral einitting bats 0.0005, perhaps it is not susprising that we (Fig. 2A), the relationship between facial found no significant relationships. How- measurements and frequency with maxi- ever, when we relaxed a to 0.05, we still mum energy is obscured. No significant failed to find any significant relation- coi-relations exist between facial rneasure- slips. This demonstrates that the lack of ments and the residuals from the frequency significance was not simply a function of with maximum energy and SIZE for each adjustment of a attributable to multipIe einission source. Likewise, two facial fea- comparisons but to a lack of strong relation- lures not correlated with SIZE - angle of Call parameters and facial features in bats Nasal (12): r2=0.46, Pc0.0154 Oral (27): r2=0.389, P<0.0005 DifferenceIn slopes: 135=3.61,P< A Emballonuridae * Hlpposideridae m Megadermatldae o Molossidae v Mormoopidae + Nycteridae A Rhlnolophldae o Rhlnopomalidae o Vespertillonldae A Emballonuridae Hipposlderldae Megadermatidae o Molossldae v Mormoopidae + Noctilionldae + Nycleridae r Phyllostomldae A Rhlnolophidae o Rhlnopomatidae o Vespertilionidae 1.8 4 4. 2.4 2.6 2.8 3.0 3.2 3.4 3.6 3.8 4.0 Length of head (In) Differencein elevatlon: ls2=7.06.PcO.0001 A Emballonuridae Hlpposlderidae X 0 -.74 . m Megademalidae 9 /' o Molossldae .=, 2.2 - v Momoopldae e Nootiilonidae t Nycleridae r Phyllostomldae A Rhlnolophldae o Rhlnopomatldae o Vespertillonldae 2.4 2.6 2.8 3.0 3.2 3.4 3.6 3.8 4.0 Length of head (In) FIG.2. Bivariate plots of echolocation frequency and morphological relationships between oral (open symbols) and nasal (filled symbols) emitting families of bats in our study. Sample size is in parenthesis. (A) Nasal emitters have a significantly higher frequency with maximum energy versus SIZE than oral emitters. (B) Oral emitting bats above the line have wider heads than nasal emitters for the same given length. The dashed regression line for all bats shows that three phyllostomids (Sphaerwzyrteris toxophyllunz, Ce~iturioserzex, and P/zyllosto17zuslzastot~rs in order from left to right) have wider heads for their length than other nasal emitters. (C) Nasal emitting bats have a significantly shorter muzzle (distance from nostril to eye) than oral emitting bats for the same head length 10 A. Goudy-Trainor and P. W. Freeman free-standing pinna to the head and number pulse from echo (Fenton et al., 1995). We of ridges on the pinna - show no correla- do not have frequencies with maximum tion with frequency with maximum energy. energy for phyllostomids or noctilionids from the literature (Table I). Phyllostoinids are low intensity callers and are difficult to record. Frequency with maximunl energy The relationship between frequency has been shown to cossespond with the fre- with maximum energy versus SIZE is such quency of best hearing in species with FM that nasal emitting bats have higher fre- calls and CFfFM calls (Schnitzler and quencies with maximum energy given their Henson, 1980; Neuweiler, 1984; Neuweiler head volume (SIZE) than oral emitting bats et al., 1984). Neuweiler et nl. (1987) (Fig. 2A). Although we followed Pedersen's demonstrated that Rhinolol~lzusrouxi, a bat I (1993) description of emission sources for that compensates for Doppler-shift, crun I families, not all families or species of bats alter the frequency with lnnxilnu~nenergy. I I are easily placed into a category. Phyllo- Differences between echolocatio~i call F stomids are generally accepted as nasal pasameters of nasal and oral elnitling bats I emitters, but Desnzodus roti~lzdushas been have not been tl~oroughly examined. I listed as an oral emitter (Schmidt, 1988). Although nasal emitting bats have higher 1 Some oral emitting bats, such as Cory. frequencies with maximum energy and gen- norhilzus towlzseizdii and Barbnstelln bar- erally higher spectral call pasalneters than 11 f I bastellus, have been shown to emit echolo- oral emitting bats, different call types :we , cation calls effectively through the nostrils used by both nasal and oral emitters. 11 (Griffin, 1958; Rydell and Bogdanowicz, Constant frequency calls and CF/FM calls 1 1997) while the nasal emitting bat, Carollia ase widespread and show little taxono~nic persptcillata, can emit echolocation calls significance (Pye, 1973). Multiharmonic orally (Griffin and Novick, 1955). FM sweeps are used for nearly every Ii Frequency with lnaximum energy which microchiropteran diet, including insects, i' 4 occurs in the outward pulse of a call has blood, vertebrate prey, nectar, pollen and been considered one of the most consistent fiuit but not lish, and all lrequency patterns t, echolocation call parameters and one of the are used lo catch insects (Pye, 19SO). h' ! most critical (Fullard et dl., 1991). Un- Mass is an especially i~nportanlSactor fortunately, it is also one of the least report- 1: anlong flying animals. In bats overall body ed parameters. However, frequency with mass is negatively correlated with freclucn- i I maximum energy is qualitatively different cy parameters, boll1 across allcl within I'nmi- in frequency modulated (FM) calls versus lies, so that smaller bats generally have constant frequency (CF) calls. In the latter higher frequency calls (Heller anil I-Iel- there is only pure tone (very narrow band of versen, 1989; Jones alld Rayner, 199 1 ; Bog- frequency also called constant frequency) danowicz et al., 1999; Jones, 1999). No and a resistance to time overlap in pulse and overall difference in body mass between echo. There is a frequency for the outward oral and nasal emitters has been reported. pulse and an upward Doppler shift in that Our study confirms differences in head frequency in the returning echo. Doppler shapes and sizes as well as differences in shifting can occur in CFIFM bats as well. frequencies with maximum energy between This is not the case in FM calls, which have nasal and oral emitters. For bats studied a broader band of frequencies and rely on here, nasal e~nittingspecies tend to Iiave time overlap of frequencies to distinguish longer, narrower heads than oral emitters, Call parameters and facial features in bats 11 although this trend does not include three facial features such as noseleaves enable pllyllostomnids (Fig. 2B). Fenton (1989) bats to send narrower bands of emissions finds that among animal-eating bats in gen- while large pinnae enable bats to have bet- eral, four nasal emitting families have pro- ter directionality of hearing than would be portionally longer heads than three oral expected from such small emitting and emitting fanzilies. This is not true for the receiving structures as is the case with bat oral emitting molossids, with longer than heads (Au, 1993). One of the most obvious expected heads, and the nasal emitting hip- facial differences between nasal and oral posiderids, with shorter than expected emitters is that nasal emitters have some heads. Freeman (2000) suggests that within type of noseleaf. No study has quantified the morphospace of strictly insectivorous, the difference between the function of a non-phyllostomid families of bats the prob- noseleaf and nostrils as opposed to the func- lem of durophagy (eating hard-shelled prey) tion of lips and mouth in echolocation emis- has been solved in different ways by oral sion. In phyllosto~nidbats, the nosereaf has and nasal emitting bats. Nasal emitting bats a wide range of sizes, but there is correspon- that eat hud items have narrower, longer dingly little variation in echolocation calls heads with vertically tall mandibular rami (Belwood, 1988; Bogdanowicz et nl., and tall sagittal crests while oral emitting 1997). Within the Rhinolophidae and Hip- bats have shorter, wider heads. However, posideridae, after controlling for size of bat, the absolute shortest, widest skulls and the noseleaf width was found to be correlated longest, nasrowest skulls are found among with frequency of strongest a11.1plitude the diverse phyllostornids (Freeman, 1998). (Robinson, 1996; see also Bogda~lowicz, Interestingly, pliyllostonlids, despite great 1992). ~norphological variation in trophic struc- Sounds returning to the bat me collected ture, all have similar echolocation calls and funneled by the external pinnae (Au, (Gould, 1977; Belwood, 1988). 1993; Obrist, 1995). Obrist et nl. (1993) Further, we can confirm that nasal elllit- found no significant correlations between Ling bats liave shorter muzzles relative to pinnal measurements and echolocation head length tl~anoral emitting bats. This paraineters across families. Obligatory car- means a shorter portion of a longer head is nivorous bats, all nasal emitters, were found occupied by the length from the eye to the to have larger ear areas than oral emitting nostril of nasal emitters (Fig. 2C). Freeman animalivorous bats (Freeman, 1984). Hen- (2000) suggests that nasal emitters need a son (1970), after reviewing several studies certain length of nasal capsule lor a proper- on the role of the pinnae in bats, concluded ly fiinctioning emission of echolocation that the pinnae's main f~lnction was to calls througl~the nose instead of tlxough the increase the directionality of the sound mouth, but we cannot confirm that idea reception system. The need for directionali- here. ty of sound reception increases with in- The wide array of notable and biz'me creasing frequency (Obrist et al., 1993). facial features within Chiroptera has raised Ears set more caudally on the head and par- questions regarding their function in tially facing laterally (outward) aide in the echolocation (Griffin, 1958). Our study collection of faint high or low frequency found no significant col-selations between echoes (Fenton, 1984; Freeman, 1984; facial features and the residuals from the Bruns et al., 1989; Obrist et a/., 1993). The frequency with mlwilnum energy and skull ridges on the inner sul-face of the pinna are size for each emission source. However, thought to reflect sound that then enters 12 A. Goudy-Trainor and P. W. Freeman the ex canal after the original echo and reading, constructive advice, statistical help, and con- could help the bat dete~minethe vertical stant support to bring this project to closure. direction of the sound source (Lawrence and Simmons, 1982). Numerous factors may interact with a mammal's echolocation system. For bats, ALDRIDGE,H. D. J. N., and I. L. RAUTENBACH.1987. some of these factors ase: the chasacteristics Morphology, echolocation and resource partition- ing in insectivorous bats. Journal of Animal of the auditory system, overall size, skull Ecology, 56: 763-778. and tooth morphology, wing morphology ALTRINGIIAM,J. D. 1996. Bats: biology and behav- and flight speed, foraging habitat, prey and iouc Oxford Universily Press, New York, 262 pp. prey availability, and facial morphology Au, W. L. 1993. The sonar of dolphins. Springer- (Fenton, 1985; Aldridge and Rautenbach, Verlag, New York, xi + 277 pp. 1987; Fullxd et oE,, 1991; Pedersen, 1993; BARCLAY,R. M. R. 1983. Echolocatio~i calls of Emballonurid bats from Panama. Journal of Kalko, 1995; Bogdanowicz et al., 1999; Conlparative Physiology, 15 1: 5 15-520. Jones, 1999). BARCLAY,R. M. R. 1984. Observations on the migra- There is considerable difference in fre- tion, ecology, and beliavior ol bals of Delta quencies of sound used by species of bats. Marsh, Manitoba. Canadian Field-Naturalist, 98: There is a general relationship between size 33 1-336. BARCLAY,R. M. R. 1986. The echolocation calls of and frequency of sound and size of bat. hoary (Lasiiirlrs cinereus) and silver-haired Howevel; the relationship between size and (Lnsiorzycteris noctivaga~ts)bats as adaptations frequency is different for nasal and oral for long- versus short-range foraging strategies emitters. Finally, there is the obvious differ- and the consequences for prey selection. Cana- ence that nasal emitters have noseleaves and dian Journal of Zoology, 64: 2700-2705. oral emitters do not. However, beyond these BAICCI-AY,R. M. 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Received 24 April 2002, accel1tetl6 Jirrze 2002