Leptonycteris yerbabuenae

Leptonycteris nivalis yerbabuenaeMartínez and Villa-R., 1940: 313. Type locality “Yerbabuena, Estado de Guerrero,” Mexico. Leptonycteris nivalis sanborniHoffmeister, 1957:456. Type locality “mouth of Miller Canyon, Huachuca Mountains, 10 mi. SSE Fort Huachuca, Cochise County, Arizona.” Order Chiroptera, family Phyllostomidae, subfamily Glossophaginae, tribe Glossophagini. L. yerbabuenae is monotypic (Simmons 2005). Leptonycteris yerbabuenae (Fig. 1) is 1 of 4 North American bats with a nose leaf. L. yerbabuenae can be distinguished from Choeronycteris mexicana and Macrotus californicus by the absence of a conspicuous tail and presence of brownish pelage in L. yerbabuenae (Arita 1999). Pelage of L. yerbabuenae is shorter and denser in comparison to the longer and fluffier pelage of L. nivalis (Davis and Carter 1962; Hensley and Wilkins 1988). L. nivalis is larger with grayish pelage, narrower uropatagium, and longer wings. L. yerbabuenae is smaller (15–25 g versus 18–30 g), has shorter wings (length of forearm 51–54 mm versus 56.5–59.5 mm), and a shorter 3rd finger (92–102 mm versus 106–115 mm) than L. nivalis (Arita 1999). Length of head and body of L. yerbabuenae averages as much as 10% shorter than that of L. nivalis at comparable latitudes (Hoffmeister 1957). Skull of L. yerbabuenae (Fig. 2) is smaller than that of L. nivalis (Davis and Carter 1962). It is shorter (mean <27 mm), the condylobasal length is usually ≤26.3 mm, and the presphenoid ridge is more prominent and more rounded than in L. nivalis (Hoffmeister 1957, 1986). Skull of L. curasoae is generally larger than that of L. yerbabuenae. Upper incisors of L. curasoae are evenly spaced and larger than those of L. yerbabuenae. Upper incisors of L. yerbabuenae occur in 2 pairs separated by a median gap (Davis and Carter 1962). Photograph of an adult female Leptonycteris yerbabuenae from Mexico. Used with permission of the photographer, M. Tuttle Dorsal, ventral, and lateral views of cranium and lateral view of mandible of an adult male Leptonycteris yerbabuenae (U.S. National Museum of Natural History [USNM] 554275) from Cochise County, Arizona. Greatest skull length is 25.9 mm Leptonycteris yerbabuenae is a leaf-nosed bat with an elongated snout. Skull has an elongate rostrum bearing a small, triangular nose leaf (Arita 1999). Skull has complete zygomata and molars are elongate with the W-shaped pattern nearly lost (Hall 1981). L. yerbabuenae has 3 caudal vertebrae but no externally visible tail (Hoffmeister 1986). Means and ranges (in mm) of external characters for 10 males and 10 females (in parentheses) from southern Arizona and Mexico are: total length, 81.8, 74–90 (75.8, 73–82); length of tail, 0 (0); length of forearm, 52.9, 51.3–55.0 (52.2, 51.5–53.5); length of 3rd metacarpal, 49.3, 48.4–51.7 (48.6, 48.0–49.5); length of terminal phalanx of 3rd digit, 10.1, 8.8–11.8 (10.7, 9.7–11.3); length of hind foot, 16.4, 15–18 (17.2, 15–19); and length of ear from notch, 17.7, 16–21 (16.8, 15–19). Means and ranges for cranial and dental measurements (in mm) for these same males and females (in parentheses) are: length of skull, 26.8, 26.0–27.3 (26.8, 26.4–27.3); width of braincase, 10.2, 9.8–10.9 (10.0, 9.8–10.2); condylobasal length, 26.5, 25.9–26.9 (26.3, 25.8–26.7); zygomatic width, 11.1, 10.7– 11.5 (10.8, 10.6–10.9); interorbital width, 5.1, 4.8–5.3 (5.0, 4.9– 5.3); mastoidal width, 10.3, 10.1–10.6 (10.3, 10.1–10.5); distance from palate to alveolus, 14.7, 14.3–15.1 (14.5, 14.1–15.0); length of mandible, 18.6, 18.3–19.0 (18.5, 18.3–18.9); mandibular depth, 2.3, 2.0–2.5 (1.9, 1.7–2.0); and length of maxillary toothrow, 9.6, 9.2–9.8 (9.5, 9.0–9.9). Mean body masses and ranges (in g) for these same males and females (in parentheses) are: 26.2, 23.5– 28.7 (24.5, 23.5–28.7). Body masses of adult males and nonpregnant females are 26.4 g and 24.9 g (Ceballos et al. 1997). Sexual dimorphism is absent (Arita 1999). Measurement (means and ranges in mm) for 5 males and 5 females (in parentheses) are: length of forearm, 53.5, 51.7–55.6 (54.7, 53.9–55.0); length of 3rd metacarpal, 47.3, 45.6–48.5 (48.8, 47.6–49.5); length of 1st phalanx III, 14.1, 13.0–14.8 (14.3, 13.4– 14.8); length of 2nd phalanx III, 23.0, 21.5–24.8 (23.9, 22.9–25.0); length of 3rd phalanx III, 11.3, 9.8–12.4 (11.5, 10.6–12.3); length of 3rd digit, 95.6, 92.1–100.3 (98.5, 95.1–101.2); condylobasal length, 25.7, 25.5–26.1 (26.0, 25.7–26.5); zygomatic width, 10.9, 10.8–11.0 (10.8, 10.1–11.3); interorbital width, 4.6, 4.3–4.8 (4.6, 4.4–4.7); mastoidal width, 10.8, 10.7–10.9 (10.9, 10.7–11.1); length of palate from alveolus, 14.2, 14.0–14.5 (14.3, 13.9–14.7); length of maxillary toothrow, 8.6, 8.5–8.8 (8.9, 8.7–9.2); and length of mandible, 18.5, 18.0–18.8 (18.7, 18.1–19.0—Davis and Carter 1962). The northern limit of the distribution of L. yerbabuenae extends from the Picacho Mountains in southern Arizona southwest to the Agua Dulce Mountains and southeast to the Chiricahua Mountains, and in southwestern New Mexico in the Animas and Pelonicillo mountains (Arita 1991; Cockrum 1991; Fleming and Nassar 2002; Hoyt et al. 1994). The range extends south from Arizona and New Mexico throughout the drier parts of Mexico, including Baja California, to Guatemala, El Salvador, and Honduras (Arita 1991; Arita and Humphrey 1988; Jones and Bleier 1974; Lee and Bradley 1992; Powell et al. 1993; Fig. 3). Geographic distribution of Leptonycteris yerbabuenae Occasional individuals have been recorded outside the northern limits of the range of the species in Arizona (U.S. Fish and Wildlife Service 1997) and in California (Constantine 1998). This species is most common below 1,800 feet in arid and semiarid habitats. L. yerbabuenae is a seasonal resident in the northern parts of its range (north of mid-Sonora), arriving somewhat earlier in southern Arizona (early April and departing mid- to late September) than in New Mexico (arriving mid-July to early September—Cockrum 1991). Occasional sightings occur during winter. Leptonycteris yerbabuenae migrates into northern Sonora and southern Arizona along 2 migration routes (Wilkinson and Fleming 1996). Lesser long-nosed bats arriving in coastal Sonora and southwestern Arizona during the spring migration travel along the western coast of Mexico. Lesser long-nosed bats arriving later in the summer to sites in south-central and southeastern Arizona and southwestern New Mexico fly along the foothills of the Sierra Madre Mountains. Migrants may travel from as far south as Jalisco (1,000– 1,600 km—Wilkinson and Fleming 1996). Late Pleistocene fossils are known from Cueva de La Presita, San Luis Potosí (= L. curasoae—Arroyo-Cabrales 1992; Arroyo-Cabrales and Polaco 2003). This locality is 21.4 km S of Matehuala, San Luis Potosí (23°29′37″N, 100°37′16″W) at an elevation of 1,540 m. Body mass in both males and females fluctuates seasonally (Ceballos et al. 1997; Galindo et al. 2004). In central Mexico, total body mass and fat deposits increased June–July in males and August–December in females when they were pregnant or lactating (Galindo et al. 2004). Almost 40% of the L. yerbabuenae examined from the Huachuca Mountains, Arizona, lacked 1 or more lower incisors (Hoffmeister and Goodpaster 1954). Structural modifications to the tongue that facilitate nectar feeding include lateral ridges (5 mm wide and 10 mm long) of long (mean of 0.9 mm), conical-shaped papillae on the tongue (Howell and Hodgkin 1976). Periodontal disease caused by the mite Radfordiella oricola is not present in L. yerbabuenae (Greenbaum and Phillips 1974) because of continual scraping of the teeth by the hooklike, filiform papillae on the tongue that prevent the attachment of Radfordiella. The large body size of L. yerbabuenae and its high wing-loading ratio facilitate energetically efficient, long-distance flight in arid habitats (Sahley et al. 1993). Estimated daily energy requirements for a nonreproductive Leptonycteris were ca. 40 kJ and 60– 80 kJ for lactating females (Horner et al. 1998). Sexual differences in flight performance and energetics influence migration strategies of males and females (Sahley et al. 1993). Mechanical power expenditure of hovering is comparable to that in slow forward flight (Dudley and Winter 2002). Lesser long-nosed bats can survive ambient temperatures up to 41°C and do not enter torpor or hibernate (Carpenter and Graham 1967). A lower basal metabolic rate, greater thermal conductance, and higher evaporative water loss permit this species to tolerate high ambient temperatures (Carpenter and Graham 1967). The lower lethal body temperature is >10°C (Carpenter and Graham 1967). Leptonycteris yerbabuenae feeds on nectar, pollen, and fruit, a diet rich in water but poor in protein and salts (Fleming and Nassar 2002). Renal papilla are very small and the medullary cortex is thick, resulting in copious amounts of very dilute urine. L. yerbabuenae normally does not drink, so does not need to roost or feed near water sources within its arid environment (Fleming and Nassar 2002). L. yerbabuenae maintains a positive nitrogen balance by ingesting pollen as its primary protein source (Howell 1974). Lesser long-nosed bats tolerate cave and mine environments with high concentrations of ammonia (>1,000 ppm, n = 1—Studier et al. 1967). Lesser long-nosed bats are often covered with pollen. They ingest this pollen in the process of grooming their fur with their feet and then licking the claws to remove the collected pollen (Howell and Hodgkin 1976). The cuticular hair scales are divergent or divaricate versus the more typical appressed condition. Erect hairs covered with these scales that project outward facilitate collection of pollen when lesser long-nosed bats visit flowers in search of nectar. Lesser long-nosed bats have bimodal hearing with greatest sensitivity at 30–40 kHz and 60–80 kHz. The external morphology of the brain is characterized by cerebral hemispheres that are short and smooth, with sulci cut deep into the mass of the cerebrum. The internal anatomy includes a short, stubby cerebrum with relatively small olfactory bulbs (McDaniel 1976). Lesser long-nosed bats do not have a dense layer of cell bodies along the margin of the interhemispheric sulcus. Leptonycteris yerbabuena hosts 2 ectoparasitic flies (Basilia antrozoi and Trichobius sphaeronotus) and 6 mite genera (Antricola, Ichoronyssus, Macronyssus, Periglischrus, Speleocola, and Ornithodoros—Bradshaw and Ross 1961; Webb and Loomis 1977). L. yerbabuenae hosts the fungi that cause candidiasis, cryptococcosis, histoplasmosis, and torulopsosis (Jones 1976; Taylor et al. 2000). Females give birth to 1 young per year, with the time of mating and parturition varying geographically (Ceballos et al. 1997; Wilson 1973). The ratio at birth is and Cockrum northern spring and southern (Ceballos et al. 1997). In males and females per The body mass of and young is g and and Cockrum of forearm and hind (in mm) for and young are 18.6, and A of short, grayish hair the body but not the head by the time the length of forearm mm and Cockrum The to fly is when the forearm mm in A pelage by the time the forearm in L. yerbabuenae and 1976). is high in g as and relatively high in fat g) and energy their lesser long-nosed bats with a protein g and protein g), young are not by of protein and 1976). In the northern of their range (north of mid-Sonora), seasonal is typical of 1991). females in mid- to late April to large of to in in Arizona and feet and near sources 1991). females to the same roost in and Cockrum L. yerbabuenae birth at the of the spring or at the of the summer (Arita Cockrum 1991). Females and young of both the roost by mid-July (Fleming and Nassar 2002). of these to males in small during the summer in southern Arizona 1991; and Cockrum and in the northern of the species range are by mating and in Mexico are separated Females at of and young of have been in northern and Cockrum females at in to the in central Mexico in birth or birth and young are ca. 6 later in northern than in southern (Fleming and Nassar 2002). In both and occur during in and in the or in are in late on San Jalisco (Ceballos et al. but south at male in (Fleming and Nassar 2002). 1 and the ca. later (Arita 1999). Leptonycteris yerbabuenae is a resident in southern Baja California with a birth the spring and birth on the (Fleming and Nassar 2002). is when flowers are in this Winter occur south of southern Sonora in and Cueva in and Nassar 2002). Females these give birth in or et al. 1986). roost has been recorded at Cueva Cueva de and and Nassar 2002). south of southern Sonora seasonal in size and A ratio and when mating but is males in (Fleming and Nassar 2002). A of L. yerbabuenae at a cave roost on near is in an that geographically the northern from the southern et al. 2003). In this L. yerbabuenae present in the cave differences in The in and in females were most in but present in and The male 2 per and et al. 2003). females and males do not have 2 per Lesser long-nosed bats have been and Cockrum of L. yerbabuenae include near roost and and have been in by lesser long-nosed bats and Cockrum In the southwestern L. yerbabuenae is in arid and (Arita 1999). In this of the seasonal in and In central and southern Mexico, the includes arid and and differences in size and are of of L. yerbabuenae (Ceballos et al. 1997; Cockrum and 1991). In the of the females at in mid- to late by and the roost is by (Ceballos et al. 1997). of the during this time are of females and and adult males can be in in late summer 1991). In a roost near size to in as males and females to the and a by late (Ceballos et al. 1997). In males and females the roost (Wilkinson and Fleming the the roost is lower in the than in the (Ceballos et al. 1997). The of L. yerbabuenae in central Mexico at seasonal in size and but females were present throughout the (Galindo et al. 2004). The in with an of males and with females during The to in as males and and the of pregnant and lactating females and their the by from its In males to the the of L. yerbabuenae in central Mexico complete their in Mexico are resident throughout the year, to et al. et al. 1996). In southern and central Mexico, seasonally with during and et al. et al. 1997; 1997; et al. et al. et al. 2000). for L. et al. are that to the northern in the spring from in at latitudes higher than or that from central mating in to in central and southern the young are and A 3rd pattern females in the same roost (Galindo et al. 2004). Leptonycteris yerbabuenae in large and to and Nassar 2002). in the size and of roost are typical and et al. et al. 1997; 1997; et al. et al. et al. 2000). of L. yerbabuenae are the (Ceballos et al. 1997). roost sites include a mine in National and Cueva Sierra Cueva La cave near Baja California San Cueva La Cueva and a cave near (Arita and Humphrey 1988; et al. 1997; Cockrum 1991; Galindo et al. et al. et al. 2003). include of and a cave near Cueva and Cueva de (Arita and Humphrey 1988; et al. 1997; Cockrum 1991). of the range of L. nivalis is within the range of L. yerbabuenae (Arita and Humphrey 1988). L. nivalis more in or and L. yerbabuenae and The 2 species along and temperature with L. yerbabuenae lower and than L. nivalis (Arita 1991). This is not complete and the ranges at The diet of L. yerbabuenae of nectar, pollen, and and Goodpaster 1954). occur in but these may have been during nectar feeding (Howell 1974). of the pollen is to nectar feeding or during grooming (Howell and Hodgkin 1976). and pollen the diet but may be when females are lactating (Fleming and Nassar 2002). Lesser long-nosed bats are and their diet with the of Leptonycteris yerbabuenae nectar and pollen from flowers and nectar, pollen, and by and in southern Arizona and Sonora (Fleming et al. 1993; and Cockrum and Wilson Winter in southern Mexico feed on flowers of a of and on their and et al. 1986). from species of is a in Mexico et al. 2003). are and the nectar is seasonally Lesser long-nosed bats time their and feeding to the of these and in the of L. yerbabuenae were (Fleming et al. 1993). L. yerbabuenae feeds on with a and during migration and in the northern of the range of the In the southern of its feeds on by L. L. yerbabuenae is a in Baja California, is a It feeds on throughout the near and are (Ceballos et al. 1997). L. yerbabuenae is a in the most arid parts of its range but a in the more (Fleming and Nassar 2002). Lesser long-nosed bats a of species that nectar during their to and from the and (Fleming et al. 1993). In lesser long-nosed bats feed on at 4 species and an species during their The for in the species is an of nectar (Fleming et al. 1993). In the nectar for the migration south is by a of L. yerbabuenae and species of and are a large (Fleming et al. 1993; and In from flowers by L. yerbabuenae more than those to Choeronycteris mexicana or to the et al. 2000). Leptonycteris yerbabuenae is a of and and of et al. 1961; and Fleming et al. and and et al. 1962). L. yerbabuenae is a of species of and is the of et al. 2003). L. yerbabuenae flowers in in habitats than in habitats. has a on lesser long-nosed bats in as as for the they et al. 2003). in by of the in the absence of L. yerbabuenae (Howell and 1981). L. yerbabuenae is an pollen for spaced (Horner et al. 1998). Lesser long-nosed bats but the of by lesser long-nosed bats is lower than that by in the same (U.S. Fish and Wildlife Service 1997). of its as an of and lesser long-nosed bats are a and the be by the of of L. yerbabuenae (U.S. Fish and Wildlife Service 1997). of lesser long-nosed bats from the and in and with and (Arita and Wilson 2002). may of lesser long-nosed bats during the when they the roost at and the within can be et al. to (Fleming et al. 1996). of in Mexico, collection of in the and for and may cause of L. yerbabuenae to Leptonycteris bats have been in the for 1976). The nectar diet the of a diet by nectar and pollen. A diet is 1976). be to protein at and at are a of the of L. yerbabuenae (Horner et al. 1998). They roost and in a In bats their roost and fly during the early with and of sources (Horner et al. 1998). In Arizona, small and (Howell individuals flowers in a large far more than to energy and (Horner et al. 1998). In southeastern Arizona, the lesser long-nosed bat diet is nectar and pollen from and 2004). strategies at L. yerbabuenae the distribution and in of with time of distance and from the and the and of flowers on the and 2004). were and flowers (Horner et al. 1998). Lesser long-nosed bats most flowers and ca. per The energy of L. yerbabuenae is to be at 40 and lesser long-nosed bats to flowers to this a energy is to by of that bats 5 in flight and fly ca. in flight of the daily time but of the energy of the time but of the energy is not during the the L. yerbabuenae in and that range in size from a to individuals (Arita 1999). when not lesser long-nosed bats roost in and 1991; Hoyt et al. 1994). They are and may a to bats (Ceballos et al. 1997; Cockrum and 1991; and Fleming 1996). In Arizona, L. yerbabuenae is the of or with Choeronycteris Macrotus M. and and Cockrum Fish and Wildlife Service 1997). In Mexico, L. yerbabuenae with 10 species of bats from 5 and Phyllostomidae, and and Fish and Wildlife Service 1997). a cave or mine with L. yerbabuenae to roost by into the cave or mine (U.S. Fish and Wildlife Service 1997). the hind feet of young are adult to from the roost the are and Cockrum lesser long-nosed bats their body into a with their and hovering the of the wings is forward and the up (Hoffmeister 1986). Leptonycteris yerbabuenae from the roost in Jalisco or high of with individuals from northern in Baja California and southern Arizona (Wilkinson and Fleming 1996). were not for bats from in and lesser long-nosed bats from the to in Baja California, and southern Arizona. from than a southern source (Wilkinson and Fleming 1996). Leptonycteris yerbabuenae has a of and a of 1967). are and in of smaller the pairs have or The is a and the is a 1967). is high of L. yerbabuenae a range of (Wilkinson and Fleming 1996). for are (Wilkinson and Fleming 1996). Leptonycteris yerbabuenae is an species throughout its range in the and Mexico, and a for this species has been (U.S. Fish and Wildlife Service 1997). L. yerbabuenae to the in 1988). It is on the of and species for Mexico de 1994). L. yerbabuenae is in the for the of of as because of resulting from range et al. In the in are relatively from to year, but on and 1991; Fish and Wildlife Service 1997; Wilson is The seasonal of migration within the northern of the range of the species be when and 1991). Fleming et al. do not that this species is or is a in in the as by its include of the lesser long-nosed loss of sites mine and for A for L. yerbabuenae and northern et al. 2003). This species is to and may not to a roost and 1991). for of lesser long-nosed bats in Mexico are western Sierra southern Sierra and the southeastern (Arita and 1999). of and for resident not in the southern of the species range is (Arita 1993). The that extends from western Mexico south into is an for this species and be (Ceballos and of within a of known as as along is (U.S. Fish and Wildlife Service 1997). The Leptonycteris is from the and in to the rostrum of this and Wilkins 1988). The to the near the small of in the of Mexico. The from a cave a short distance south of somewhat higher than 1,800 and near a locality and L. yerbabuenae in a of to this species can be the L. from L. yerbabuenae is more and has a much distribution than the species in the (Arita and Humphrey 1988). Arita and Humphrey that L. nivalis is than and that L. nivalis to L. yerbabuenae. The of this for because most of the of L. nivalis yerbabuenae lost the Arita and Humphrey examined 3 and that L. yerbabuenae on a of that both nivalis and yerbabuenae. They for including yerbabuenae in the of L. a species known from and the including and and separated yerbabuenae and to the of 3 species and