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Seasonal shifts in the diet of the big brown bat (Eptesicus fuscus), Fort Collins, Colorado.

The distribution of the big brown bat (Eptesicus fuscus) is widespread across North America (Hall, 1981). Throughout its distribution, many studies have examined the diet of this species (Hamilton, 1933; Phillips, 1966; Ross, 1967; Black, 1972, 1974; Whitaker, 1972, 2004; Whitaker et al., 1977, 1981; Brigham and Saunders, 1990). Although researchers have found a wide variety of prey items to comprise the diet of E. fuscus, it is generalized that this species feeds primarily on beetles and other hard-bodied arthropods (Whitaker, 1972). Black (1974) found that the diet of E. fuscus from New Mexico comprised mostly coleopterans and categorized this bat as a beetle strategist. However, Brigham and Saunders (1990) found that E. fuscus in the Okanagan Valley, British Columbia, fed mostly on Trichoptera, and less on coleopterans. Verts et al. (1999) also found that Trichoptera was a substantial part of the diet for E. fuscus but concluded that this prey item was likely selected because the maternity colony sampled fed along a riverine area.

Moosman et al. (2012) found that the diet of E. fuscus from New England comprised mostly coleopterans (81% volume) during the summer months, and through meta-analyses concluded that E. fuscus from the eastern United States and northern latitudes of western North America that included Oregon, Alaska, and Canada, shared similar trends in beetle consumption. However, they noted that there was a greater presence of coleopterans and fewer lepidopterans in eastern regions. Moosman et al. (2012) found general longitudinal differences in diet of E. fuscus across North America with greater consumption of beetles in the east, and similar patterns on a smaller scale in Oregon, with greater beetle consumption in the eastern part of the state. Moosman et al. (2012) concluded that climate was likely a driving force in the abundance of certain prey items in the diet of E. fuscus, with a trend to greater use of beetles and decreased use of lepidopterans with increasing temperature. They suggested that big brown bats from the western United States may follow a more generalist pattern in feeding behavior, but acknowledged the paucity of information on the diet of these bats from this region.

During spring and autumn of 2002, unusually large swarms of miller moths or adult army cutworms (Euxoa auxiliaris) moved through our study area at Fort Collins, Colorado (Cranshaw, 2006). We hypothesized that these moths would be a readily available resource for a variety of opportunistically feeding vertebrates, including E. fuscus. According to Ross (1967:224), E. fuscus "does not prey upon moths to an appreciable degree." However, the more recent study by Moosman et al. (2012) suggests that E. fuscus in the western United States might indeed show greater breadth in their consumption of insect prey. We hypothesized that E. fuscus would be opportunistic in their feeding behavior at our study area and would take advantage of the seasonal availability of miller moths. Our objectives, therefore, were to determine if the diet of E. fuscus sampled at Fort Collins, Colorado, varied seasonally with the availability of miller moths, and if prey consumption followed the pattern of increasing use of beetles with seasonally warmer temperatures as predicted by Moosman et al. (2012). We also sought to determine if beetle consumption might decrease during the post-reproductive period of big brown bats at our study area because increased agility of nonpregnant bats might reduce their dependence on these slower, more direct-flying prey. Studies on other species of temperate-zone bat diets suggest that pregnant bats with lower agility may favor beetles over moths (Valdez and Cryan, 2009).

MATERIALS AND METHODS--We netted bats from 17 May-20 September 2002, at five sites within Fort Collins, Colorado (40[degrees]35'7"N, 105[degrees]5'2"W, elevation 1,525 m; see O'Shea et al., 2011 for more detailed description of the study area in relation to the bat community). We netted from approximately 1900h-midnight and captured 30 individual big brown bats (25 adult and 2 juvenile females, 3 adult males). Nearly all big brown bats captured at Fort Collins were individually tagged through insertion of passive integrated transponders (Wimsatt et al., 2005) as part of a larger study (e.g., George et al., 2011; O'Shea et al., 2010, 2011). We held bats individually in small bags for approximately 10 min to collect guano. The amount of guano collected from each bat ranged from one to eight fecal pellets. We regarded each bat as one sample unit regardless of number of pellets. We separated data into seven sampling periods based on dates of collection and net capture sites. Sampling periods were separated by approximately [greater than or equal to] 7 days, except for samples collected on 17 May and 20 May 2002, to provide a general grouping relative to seasons. All samples included a single date of sampling except for the capture of one bat each on 21 May and 29 May. We grouped these with 20 May and 28 May samples at the same net sites.

We examined fecal samples following techniques described by Whitaker (1988) and Whitaker et al. (2009). This included dissecting fecal pellets moistened in a petri dish with 95% ethanol under a 10-60-power zoom microscope. We identified most prey items to the lowest possible taxonomic level, usually to family. However, we could not identify some fragments in the guano, such as those representing Lepidoptera (moths), lower than order. We found keys, general morphological descriptions, distributional occurrences, and related natural history information in relevant literature (i.e., Borror and White, 1970; White, 1983; Whitaker, 1988; Borror et al., 1989; Arnett, 2000; Arnett and Thomas, 2001; Arnett et al., 2002; Triplehorn and Johnson, 2005). We also used insect specimens housed in the Museum of Southwestern Biology, Albuquerque, New Mexico, as reference material for the identification of some fragments found in guano. We sought expert insight from entomologists at the Museum of Southwestern Biology. We retained the traditional use of Lygaeidae (Borror et al., 1989) instead of an alternative taxonomic division into 10 distinct families within Hemiptera (Triplehorn and Johnson, 2005).

We visually estimated volume percentages of prey types for each sample and categorized them by taxonomic group. Summed volume percentages within each sample equaled 100%. in instances where more than one sample represented a sampling period (e.g., n = 5 for 17 May), we calculated an average of volume percentages for each prey item. If sampling periods contained more than one identified family of insect of the same order, we calculated a sum of volume percentages to represent total volume percentage of that order. In addition, we calculated frequencies of occurrence by counting number of samples representing a particular insect prey item within a sampling period and dividing by the total number of samples within that sampling period. If more than one insect family within the same order was represented per sample, we counted representatives of that insect order as one representative for that sampling period, then divided by the total number of samples within that sampling period and multiplied by 100. Because sample sizes were small, we pooled sexes (27 of 30 were female). The subdivision of the sample of 30 bats by sampling dates, sex, age, or other factors would preclude statistical analysis; results are simply presented as volume percentages (% volume) and frequency of occurrence (% frequency) pooled by date.

We compared diet with temperature and precipitation data at the time of sampling from the Fort Collins, Colorado, meteorological station, available from Western Regional Climate Center (2012). We also compared dietary habits with reproductive conditions of netted female bats, as well as with the reproductive conditions of female big brown bats examined at multiple roosts in Fort Collins, to determine if there was a trend in feeding strategies and reproduction. Reproductive condition of females was diagnosed by palpation and external examination (pregnant, lactating, postlactating, nonreproductive; O'Shea et al., 2010).

RESULTS--Big brown bats fed mostly on lepidopterans (moths) and dipterans (flies) during the 17-20 May sampling periods (Table 1). Two major insect orders were consumed: lepidopterans dominated the diet at 81-83% volumes, and dipterans comprised the remainder at 17-19% volumes (Table 1). On 28 May coleopterans were dominant in abundance (76% volume) and occurrence (100% frequency; Table 1). Dipterans, however, remained similar in percentage of volume and frequency. Unlike on 17 and 20 May, bats consumed additional insect orders during 28 May, including hymenopterans and hemipterans, but only at 1% volume or less and were encountered in only 33% of the samples (Table 1). Temperatures reached warmer daily maxima on 28 May than on the earlier two sampling dates. The temperature ranges on 17 and 20 May were 6.7-15.0[degrees]C and 7.8-17.8[degrees]C, respectively; on 28 May temperatures were 7.8-27.8[degrees]C. We examined 39 individually tagged adult female bats in Fort Collins from 17-31 May 2002: 35 (90%) were pregnant. Ten of 14 bats sampled for guano in May were pregnant (71%); 4 were nonreproductive or were too early in pregnancy to accurately diagnose.

Beetles continued to be the major prey item in guano sampled 23 July-9 August (at 74% volume or greater and in all samples examined), whereas lepidopterans (8% volume, 60% frequency) were found only in samples from 9 August (Table 1). Unlike the samples from May, dipterans comprised smaller portions of the diet (i.e., 6% volume or less) for bats sampled during 23 July-9 August. Within Coleoptera, we identified several prey itemsto family, including Carabidae, Chrysomelidae, Curculionidae, Dytiscidae, and Scarabaeidae. There appears to be a trend among the presence of these beetles at 25% or greater volume in the diet of E. fuscus, with overlapping presence of these values across sampling periods. For example, scarabaeids were present at 63% and 64% volumes for the respective 28 May and 23 July samples; followed by the overlapping curculionids at 25% and 42% volumes for 23 and 31 July, respectively; and then carabids at 40% and 65% volumes for 31 July and 9 August, respectively (Table 1). The single sample analyzed for 20 September comprised mostly Lepidoptera at 99% volume and 100% frequency, with trace amounts of Coleoptera at 1% volume, 100% frequency. Temperatures on the three sampling nights in July and August ranged 12.8-15.6[degrees]C minimum and 28.3-36.7[degrees]C maximum. On 20 September the minimum and maximum temperatures were 5.0[degrees]C and 26.7[degrees]C, respectively. We determined reproductive status of 205 individual adult females from maternity colonies in Fort Collins between 23 July and 9 August (see O'Shea et al., 2010). Nearly all (201, or 98%) were postlactating or nonreproductive. Eight of 14 bats netted and sampled for guano in July and August were adult females, all postlactating or nonreproductive. The bat sampled on 20 September was a nonreproductive young-of-the-year female. During the sampling dates, only 17 May had any recorded amount of precipitation (0.33 cm).

DISCUSSION--We documented five orders and nine families of insects in our analyses of guano collected from E. fuscus in Fort Collins, Colorado during 2002. Many of these insects are characteristic of the foraging habitat (riparian vegetation and associated aquatic areas) used by E. fuscus at the study area as determined by radio-tracking (O'Shea et al., 2011) as well as at the specific areas where we sampled bats. Such habitats are likely home to some of the insects (e.g., Chrysomelidae [leaf beetles], Dytiscidae [predaceous diving beetles], and Hemerobiidae [brown lacewings]) consumed by E. fuscus. However, we also found what appear to be seasonal shifts in the diet of E. fuscus across the period of 17 May-20 September. These dietary shifts included changes in consumption of type of insect, i.e. soft-bodied (moths) vs. hard-bodied (e.g., beetles), as well as changes in dietary diversity over time. Eptesicus fuscus sampled in 2002 consumed strictly soft-bodied insects from 17-20 May, then later transitioned to hard-bodied insects during 28 May-9 August, and eventually appeared to return to a dominant prey item of soft-bodied insects on 20 September. The diversity of insects consumed also followed similar trends related to corresponding sampling dates, with two orders of insects consumed by E. fuscus earlier in the year (i.e., 17 May), then peaking at five orders and six families of insect on 9 August, and concluding with two orders of insects consumed at the end of the summer on 20 September. The general presence of more moths and flies in their diet seems to coincide with cooler temperatures.

A large presence of miller moths at the study area during the spring of 2002 coincided with the phenology of lepidopterans in the diet of big brown bats. Adult miller moths pupate on the eastern plains of Colorado from March-May and migrate westward to higher elevations (Cranshaw, 2006), then in the autumn migrate back to their breeding areas on the plains (Powell and Opler, 2009). Flights of miller moths generally last about 5 to 6 weeks around mid-May-early June during years of outbreaks, but this can vary (Cranshaw, 2006). In 2002, "nuisance numbers" of miller moths occurred along the Front Range region of Colorado (including Fort Collins) over an extended period of time from late April-early July (Cranshaw, 2006). Although we were unable to identify moths to lower than ordinal level, we believe that Euxoa auxiliaris composed the bulk of the moths consumed by Eptesicus fuscus. If true, then our study provides support for opportunistic feeding behavior of E. fuscus. Likely consumption of these moths by E. fuscus also provides evidence that this bat may have an impact on a pest species whose larvae (army cutworms), as noted by Powell and Opler (2009), are potential threats to cereal crops in the Great Plains and western North America.

Cooler temperatures are associated with the spring and autumn occurrence of moths, and warmer temperatures appear to coincide with the presence of beetles in the diet of E. fuscus at Fort Collins. We believe that because of their ectothermic physiology, beetles may require relatively constant and warmer temperatures of summer to be volant. Periods of warm temperatures may also coincide with the dispersal for foraging of certain beetles (e.g., chrysomelids, scarabaeids). However for dytiscids as reported for 31 July (Table 1), warm ambient temperatures may not directly influence their physiology because of their aquatic habitat. Although many can fly (White, 1983), the volant behavior of these primarily aquatic beetles is associated with colonizing new habitat, searches for overwintering sites, or dispersal due to habitat alteration such as desiccation (Larson et al., 2000). Depending on the period of time when these movements occur, cooler temperatures would have a greater impact on the flight activity of these beetles (K. B. Miller, pers. comm.).

Although there was a greater presence of beetles in the diet that coincided with warmer temperatures of summer, miller moths were still abundant in the area during early summer of 2002 (Cranshaw, 2006). Nonetheless, moth consumption by E. fuscus shifted to beetles and other prey types by late May. This change in prey type coincides not only with warmer temperatures but also with the period of pregnancy in E. fuscus from Fort Collins. This shift in consumption of prey type by reproductive females occurs in other temperate bat species of North America. For example, Valdez and Cryan (2009) documented a similar trend of moth consumption, in greater volumes, by hoary bats (Lasiurus cinereus) migrating northward through New Mexico during the spring, followed by fewer moths present during late spring and early summer. They concluded that beetle consumption by hoary bats in Canada, a destination point of northward-migrating bats during June (Barclay, 1985; Rolseth et al., 1994), was related to the flight abilities of near-term pregnant females during later months. Given the energetic costs of flight for pregnant insectivorous bats (Cryan and Wolf, 2003), it is likely that E. fuscus consume beetles during the warm early summer because of the slower and less maneuverable flight abilities of these insects compared to moths. However, it is important to note that the feeding strategy of E. fuscus at our study area continued to consist largely of beetles even during the postlactating phase of the reproductive cycle when bat agility should be high.

In general, many studies (e.g., Black, 1972; Whittaker, 2004; Moosman et al., 2012) of the food habits of E. fuscus throughout North America have shown that the diet of this bat is comprised mostly of beetles and other hard-bodied insects, with a low presence of moths or other soft-bodied prey items. Interestingly, many of the samples in these studies were collected in summer months. According to our data from July and August, this summer trend in diet also holds true for E. fuscus at Fort Collins. However, the diet of E. fuscus at our study area before or after this summer period was strikingly different, and showed seasonal shifts. Eptesicus fuscus does not consume strictly beetles but instead may be seasonally opportunistic in its feeding behavior relative to insect prey availability and location. However, when preferred prey items such as coleopterans are available, the bats select for that prey item.

In the study by Moosman et al. (2012), beetle consumption was greater for E. fuscus in the eastern United States (e.g., West Virginia) that had wetter habitat and warmer temperatures, but changed longitudinally when compared to bats from the Northwest (e.g., Oregon), which consumed more moths than beetles from drier habitat with cooler temperatures. Given the central location of our study area relative to the areas examined by Moosman et al. (2012) and because our sampling periods coincided with a severe drought in Colorado (Pielke et al. 2004), we found it difficult to determine if our results followed the same longitudinal trend. It is possible that subsequent years that do not include severe drought conditions may provide better insight on dietary trends of E. fuscus from Colorado relative to broad-scale patterns reported by Moosman et al. (2012). In addition to examining longitudinal climate and dietary data, we believe that latitudinal trends, similar to those reported for Myotis occultus from Colorado and New Mexico (Valdez and Bogan, 2009), should be considered for understanding the diet of E. fuscus throughout its distribution.

In agreement with Moosman et al. (2012), we feel that to better understand the feeding habits of E. fuscus, it is equally important to understand the phenology of insects. Our data also concur with their findings that temperature appears to have an association with type of prey consumed. Therefore, future studies on feeding habits of E. fuscus and other insectivorous bats in temperate regions should explore the diet over a greater seasonal breadth, and should investigate or incorporate information related to local climate data, insect phenology, and reproductive conditions of female bats.

Special thanks to K B. Miller at the Museum of Southwestern Biology, University of New Mexico, for insight and expertise on arthropods, particularly aquatic beetles. Thanks to the Division of Arthropods at the Museum of Southwestern Biology for use of reference material. We thank L. Ellison, D. Grossblat, B. Iannone, J. Laplante, H. Lookingbill, G. Nance, D. Neubaum, M. Neubaum, R. Pearce, and V. Price for help in sampling bats in 2002.


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Submitted 7 September 2012.

Acceptance recommended by Associate Editor, Stephen G. Mech, 20 March 2014.


United States Geological Survey, Department of Biology, MSC03 2020, 1 University of New Mexico, Albuquerque, NM 87131-0001 (EWV)

United States Geological Survey, Fort Collins Science Center, 2150 Centre Avenue, Building C, Fort Collins, CO 80526-8118 (TJO)

TABLE 1--Insects consumed by big brown bats (Eptesicus
fuscus) from Fort Collins, Colorado, that were sampled
during 2002 netting efforts. Values for insect prey
represent volume percentages; frequencies of occurrence
are in parentheses.

Insect prey       % Volume (% frequency of occurrence)
                  of insect prey

                   17 May     20 May     28 May    23 July
                  (n = 5)    (n = 7)    (n = 3)    (n = 4)

Lepidoptera       81 (100)   83 (100)   <1 (67)     -- (a)
Diptera           19 (100)   17 (71)    15 (100)    4 (25)
Hymenoptera          --         --      <1 (33)       --
Hemiptera            --         --       1 (33)       --

  Lygaeidae          --         --       1 (33)       --
  Pentatomidae       --         --         --         --
  Cicadellidae       --         --         --         --

Neuroptera:          --         --         --         --
Coleoptera           --         --      76 (100)   98 (100)

  Carabidae          --         --         --         --
  Chrysomelidae      --         --         --       8 (25)
  Curculionidae      --         --         --      25 (25)
  Dytiscidae         --         --         --         --
  Scarabaeidae       --         --      63 (67)    64 (75)
  Unknown            --         --      13 (33)     1 (50)

Unknown insect       --      <1 (<1)       --         --

Insect prey       % Volume (% frequency of occurrence)
                  of insect prey

                  31 July    9 August   20 September
                  (n = 5)    (n = 5)      (n = 1)

Lepidoptera          --       8 (60)      99 (100)
Diptera            1 (60)     6 (60)         --
Hymenoptera        9 (20)       --           --
Hemiptera          1 (40)    13 (100)        --

  Lygaeidae        1 (40)     3 (60)         --
  Pentatomidae       --       2 (20)         --
  Cicadellidae       --       8 (40)         --

Neuroptera:       <1 (20)    <1 (20)         --
Coleoptera        89 (100)   74 (100)     1 (100)

  Carabidae       40 (60)    65 (100)        --
  Chrysomelidae      --         --           --
  Curculionidae   42 (80)     9 (20)         --
  Dytiscidae      <1 (20)       --           --
  Scarabaeidae     6 (20)       --           --
  Unknown         <1 (20)    <1 (20)      1 (100)

Unknown insect    <1 (20)    <1 (20)         --

(a) Dash indicates not found.
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Author:Valdez, Ernest W.; O'Shea, Thomas J.
Publication:Southwestern Naturalist
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Date:Dec 1, 2014
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