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Sex ratio of rodents as barn owl (Tyto alba) Prey.


Research on the sex ratio of rodents has included examination of sex ratios of rodents identified in owl pellets (e.g., Terman and Sassaman, 1967; Myers and Krebs, 1971 ; Clark and Wise, 1974; Holt and Williams, 1995). Some authors have suggested owls select one sex of prey over the other {e.g., Dickman et al, 1991), whereas other authors have suggested unequal sex ratios of prey in owl pellets may be due to sexual differences in susceptibility to predation (e.g., Boonstra, 1977; Longland and Jenkins, 1987). Herein we describe the sex ratios of the two most abundant prey taxa in a sample of ~120 barn owl (Tyto alba) pellets.

Pellets were collected from a corrugated tin farm-equipment shed enclosed on three sides and the top with an opening approximately 15 m wide and 5 m high. Located in southeastern Washington slate (46[degrees]19.591'N, 118[degrees]00.182'W), the shed sat on an artificially leveled area in the bottom of a shallow, steep-sided, south-draining canyon. Vegetation in the canyon included a dense stand of ~2 m tall grass {Agropyron sp., Promus sp., Poa sp.) with a few scattered trees (Pinus sp.), shrubs (Rosa sp.), and forbs. Most of the canyon slopes were used as horse pasture from the 1970s through 2010. All ridges defining the canyon edges were wheat fields in production from the 1970s through the 1990s. For purposes of soil conservation, in the autumn of 2000 the northwest-ridge field, approximately 20% of the land area (25 ha) in the immediate environment of the shed, was placed in a soil bank and remaining wheat stubble was seeded to bluebunch wheatgrass (Pseudoregneria spicata), slender wheatgrass (Agropyron trachycaulum), big bluegrass (Poa ampla), and Indian ricegrass (Oryzopis hymenoides). By July 2001, this field had a patchy stand of grass. Areas of partially deteriorated field residue, without green vegetation cover, existed on ~30% of the field. By 2006, most of the field residue had deteriorated or been removed by wind and relatively continuous grass cover existed over ~95% of the field.

Pellets were collected in 1999, 2000, 2001, 2009, and 2011. We refer to the combined 1999 and 2000 pellets (n ~ 63) as the "agricultural" sample and the combined 2001, 2009, and 2011 pellets (n ~ 57) as the "soil bank" sample. Previous analyses of the fauna in the owl pellets found (i) the most abundant prey were deer mice (Peromyscus manirulatus) and microtines (Microtus spp.) (Table 1), (ii) most of these two taxa were skeletally immature individuals (Lyman et al, 2001 ; Lyman, 2012), and (iii) the difference between the agricultural sample and the soil bank sample involved a shift from deer mice as the most abundant taxon in the former to voles in the latter (Lyman, 2012). This aligns with local habitat usage by voles and deer mice (e.g., Randall and Johnson, 1979; Kaufman et al, 1988; and Falls et al, 2007, respectively). It also reflects the fact that barn owls are opportunistic feeders (Smith et al, 1972; Marti, 1988; Marra et al, 1989), therefore remains of prey in their pellets tend to reflect the small mammal fauna on the landscape (Hadly, 1999; Terry, 2010; Heisler et al, 2016).

We did not know what the rodent population on the landscape around the shed was like. We initially suspected females would be more abundant than males in the general populations of both taxa as a result of agricultural tillage destroying nests, cover, and burrow systems (e.g., Witmer et al, 2007) and surviving females adjusting their reproduction to favor females in order for the population to increase (or at least remain static). Previous research showed that microtines tend to produce more females than males when population density is low (Lambin, 1994; Bond et al, 2003; Bryja et al, 2005). After tillage was reduced by converting some land to soil bank, and population density increased, we suspected the sex ratio would become more even.


Upon collection, pellets were placed in plastic bags and transported to the Zooarchaeology Laboratory at the University of Missouri-Columbia (MU), where they were stored at room temperature and numbered. Each pellet was soaked in water for ~30 min, disaggregated, and faunal remains were removed using a dental pick and tweezers. All bones and teeth were placed in a plastic vial labeled with the pellet number. Faunal remains and data described herein are curated in the Zooarchaeology Laboratory, MU.

Identification of the species regurgitating the pellets was based on the large size of the pellets (5-6 cm long, 2.5-3 cm in diameter), oval shape, and sighting of a large owl leaving the shed in 1999. These attributes suggested barn owls (Tyto abla) were responsible for the pellets (Wilson, 1938; Moon, 1940). Also, the relatively complete skeletons with anatomically intact bones suggested barn owls were likely responsible for the pellets (Dodson and Wexlar, 1979; Hoffman, 1988; Andrews, 1990; Kusmer, 1990).

We determined the minimum number of individual (MNI) rodent prey present based on the most abundant skeletal element among left mandibles, right mandibles, left maxillae, and right maxillae. The MNI is a minimum because three left and four right mandibles represent a minimum of four individuals, butas manyas seven individuals actually might be represented (Grayson, 1984; Lyman et al, 2003; Lyman, 2008). We lacked the ability to anatomically match bilateral pairs of skeletal elements (e.g., Lyman, 2006), therefore the frequency of individuals typically is a minimum (Grayson, 1984; Lyman, 2008).

To determine the sex of rodent prey in the pellets, we first identified all deer mouse, microtine, and western harvest mouse (Reithrodontomys megalotis) innommates. Because we could not distinguish the innominates of these three genera (e.g., Clark and Wise, 1974), we lumped them all together for this analysis. Remains of western harvest mouse were identified in only the soil bank pellets (Table 1). The relatively few harvest mice represented (n = 16; 3.7%) out of a combined sample of deer mice, microtines, and harvest mice (n = 436) suggested our results would not be unduly skewed by inclusion of harvest mice in our analysis. We discuss our results as pertinent only to deer mice and microtines.

Because we could not determine which left innominate went with which right innominate, we examined all innominates regardless of side. Of 585 specimens, 522 innominates were anatomically complete; only complete innominates were included in our analyses. We measured three dimensions of each complete innominate following Dunmire (1955): length of the ischium--"from the posterior angle of the ischium to the nearest edge of the acetabulum," length of the pubis--"from the ventral apex of the pubis (i.e., the pubic symphysis) to the nearest edge of the acetabulum," and width of the pubis--"the thinnest width of the pubis." Each measurement was recorded by use of digital calipers and rounded to the nearest tenth of a millimeter. Equal numbers of innominates were measured by each of three of us and no systematic differences were found between individuals (e.g., Lyman and VanPool, 2009).


Dunmire (1955) found that a bivariate scatterplot of the ratio of the pubic length to the ischium length against the pubic width separated male from female innommates of Peromyscus and Microtus. He reported the means and ranges for each variable. We omitted 5 innominales from our analysis that greatly exceeded (>2.0) the range of the pubis length/ischium length ratio observed by Dunmire ([less than or equal to] 1.58 for Peromyscus; [less than or equal to] 1.70 for Microtus). These specimens are quite small and seem to represent exceptionally young animals, hence the size ratio may be misleading as to the sexes of the individuals. Their omission from our analysis does not influence our results or conclusions.

Dunmire (1955) did not suggest the specimens of known sex he measured represented all possible sex-related variability in innominate dimensions. However, he perceived no difference between two subspecies of Microtus californicus. Further, Clevedon-Brown and Twigg (1969) and Longland and Jenkins (1987) found the dimensions Dunmire measured were robust indicators of individual sex across several rodent genera, and the former also noted that the ontogenetic age of individual animals did not seem to skew the diagnostic value of the skeletal dimensions measured.

We superimposed Dunmire's (1955) taxon-specific empirically derived lines separating the two sexes on a bivariate scatterplot of the same two variables as measured on innominates from our owl pellets (Fig. 1). When measurements for an innominate from an owl pellet fell in the "male" area of Dunmire's (1955) data, we recorded that innominate as male; innominates from owl pellets that fell in the "female" area of Dunmire's graph were recorded as female. Because separation of the sexes in the two genera differs slightly, we did not assign innominates from owl pellets to a sex category that fell between Dunmire's taxon-specific lines separating the sexes.


Of 517 anatomically complete, measureable innominates, 451 (87.2%) clearly fell within the male or female area of Dunmire's graphs; 66 could not be unambiguously assigned to a sex category (Fig. 1). Male innominates (n = 139) were significantly less abundant than female innominates (n = 312) in the complete set of pellets (all five annual samples, 30.8% male, 69.2% female; chi square = 66.36, P < .0005). There was no statistically significant difference between the sex ratios of rodents in the agricultural sample (n = 272 sexable innominates, 31.6% male:68.4% female) and the soil bank sample (n = 179, 29.6%:70.4%; arcsine [t.sub.s] = 0.449, P > 0.5).


Because the ratio of deer mice to voles shifted from 3.1:1 to 0.45:1 (Table 1) coincident with the shift from more agricultural land to more nonfilled soil bank land, stasis in the sex ratio is not the result of taxonomic similarities of the two samples. This suggested the sex ratios of both taxa did not change when land use changed. No significant change in sex ratios of the common vole (Microtus arvalis) was found when a European agricultural field was no longer tilled and seeded and became weedy (Janova et al., 2008). Alternatively, perhaps the sex ratio for deer mice was originally female dominated and it became more even when land use changed. At the same time, perhaps the ratio for microtines was more even during the agricultural phase but became more female dominated when land was put in soil bank (or vice versa). We must determine how to distinguish innominates of the two genera in order to determine which of these alternatives applies.

A number of hypotheses explaining unequal sex ratios in rodent populations have been advanced (e.g., Bond et al, 2003). These include local resource competition, the sex ratio of the population at the time of reproduction, the first cohort selective advantage, and others. Observations on reproduction in the wild of several vole species indicate greater numbers of females born in the spring and early summer and greater numbers of males born in the late summer and autumn. Researchers suggest this pattern results because it allows females to breed prior to the coming winter and males to breed the following spring (e.g., Jannett, 1981; Lambin, 1994; Bond et al, 2003; Bryja et al, 2005). Whether the females > males ratio is the result of female manipulation of the sex ratio of their offspring (Bond et al, 2003), sex-based variability in recruitment and survival (Bryja et al, 2005), population density and the nature of interaction between philopatric females (Lambin, 1994), or dominant males disallowing subordinate males to breed (Jannett, 1981) is less clear. Reproduction in the wild among deer mice tends to produce either equal numbers of males and females (Kaufman and Kaufman 1982), more males than females (Terman and Sassaman, 1967), or to fluctuate somewhat randomly (Havelka and Millar, 1997; Stewart et al, 2014).

Longland and Jenkins (1987) found more female than male rodents in a collection of owl pellets. They hypothesized that because females were more crepuscular than males, they were more likely to be taken because barn owls forage more efficiently during dawn and dusk (Dice, 1945). They further suggested subordinate females may have been displaced by superordinate males, thus spent more time in open habitats, making them more vulnerable to owl predation (see also Dickman et al, 1991; Holt and Williams, 1995).

Barn owls are opportunistic foragers (Marra et al, 1989) and have greater foraging success when vegetation is patchy and open (Wooster, 1936; Kirkpatrick and Conway, 1947; Fast and Ambrose, 1976; Dickman et al, 1991). Whether female rodents were more abundant than males on the landscape when the owls were foraging is unknown. Intraspecific (between males and females of a species) and interspecific (voles displace deer mice) interactions of rodent prey likely more often resulted in juvenile females of both deer mice and voles being displaced into more open habitats, of either agricultural fields or soil bank grasslands. Thus, young females of both species of rodents would have been more available to foraging barn owls than males.

Acknowledgments.--We thank K. E. Lyman and the late R. J. Lyman for access to their equipment shed over the years. Comments on an early draft were provided by L. Carraway, G. L. Daskalakis, O. H. Perez, S. Wolverton, and two anonymous reviewers. We dedicate this paper to Sophie Kerassidou Daskalakis.


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R. LEE LYMAN (1), ANDES E. DASKALAKIS-PEREZ, ARES B. DASKAIAKIS-PEREZ, and ECO A. DASKALAKIS-PERF.Z, Department of Anthropology, 107 Swallow Hall, University of Missouri, Columbia 65211. Submitted 6 November 2015; Accepted 8 April 2016.

(1) Corresponding author: e-mail:
TABLE 1.--Frequencies (minimum numbers of individuals) of prey
identified in -120 barn owl pellets collected in southeastern
Washington in 1999-2011. Pellets were subdivided based on primary
plant cover at the time of collection, which was agricultural crops
in 1999-2000 and soil bank vegetation in 2001-2011

Taxon                      Common name      1999-2000   2001-2011

Reithrodontomys          Western harvest                   16
megalotis                mouse

Peromyscus maniculatus   Deer mouse            184         58

Micro tus sp.            Vole                    5         30

Microtus longicaudus     Long-tailed vole                  13

Micro tus montanus       Montane vole           54         76
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Title Annotation:Notes and Discussion Piece
Publication:The American Midland Naturalist
Article Type:Report
Geographic Code:1U9WA
Date:Jul 1, 2016
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