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Article

Burrowing Owls Require Mutualist Species and Ample Interior Habitat Space

by
K. Shawn Smallwood
1,* and
Michael L. Morrison
2
1
Independent Researcher, 3108 Finch Street, Davis, CA 95616, USA
2
Department of Rangeland, Wildlife, and Fisheries Management, Texas A&M University, College Station, TX 77843, USA
*
Author to whom correspondence should be addressed.
Diversity 2024, 16(9), 590; https://doi.org/10.3390/d16090590
Submission received: 1 August 2024 / Revised: 2 September 2024 / Accepted: 12 September 2024 / Published: 19 September 2024
(This article belongs to the Section Biodiversity Loss & Dynamics)
Browse Figures
Versions Notes

Abstract

:
Mitigating habitat loss of western burrowing owls (Athene cunicularia hypugaea) often involves relocation from California ground squirrel (Otospermophilus beecheyi) burrows to offsite nest boxes. Naval Air Station Lemoore (NASL), Kings and Fresno counties, California, initiated this approach to displace a regionally important population from airfield grasslands. We examined monitoring data of burrowing owls and fossorial mammals at NASL to assess mitigation options. Occupied nests increased by 33 (61%), with 47 nest box installations in 1997–2001, peaked at 87 in 1999, then declined by 50 through 2013. Although ≥13 nest boxes were occupied in 2000, none were occupied in 2003–2013. Within a 43.1 ha isolated grassland monitored for 13 years, nest site reuse in ground squirrel burrows averaged only 17% between any 2 consecutive years. Compared to the average density across grassland study areas, ground squirrel burrow systems/ha numbered 43% higher within 60 m of occupied nests and non-breeding-season burrows. Vegetation clearing to restore kangaroo rat (Dipodomys n. nitratoides) habitat preceded a 7.4-fold increase in ground squirrel burrow systems and a 4-fold increase in occupied nests, but drought-induced extirpation of ground squirrels eliminated occupied nests from the 43.1 ha grassland study area. Ground cover near occupied nests averaged 58% of the mean vegetation height and 67% of the mean percentage of bare ground in the field. Both nest sites and non-breeding-season burrows occurred >60 m interior to field edges 1.4 times more than expected. Non-breeding-season burrows averaged 328 m from same-year nest sites, and only 7% of non-breeding-season burrows were also used as nest sites. Mitigating habitat loss should be made more effective by fostering natural burrow construction by fossorial mammals on patches of short-stature vegetation that is sufficiently expansive to support breeding colonies of ≥12 pairs averaging ≥60 m from the field’s edge and a separation between non-breeding-season burrows and nest burrows minimally equal to mean nearest-neighbor distances among nests.

1. Introduction

The western burrowing owl (Athene cunicularia hypugaea) has declined in abundance and distribution [1,2,3,4,5], including within California’s southern Central Valley, which supported one of the largest concentrations of burrowing owls in California [6,7,8]. Following rapid, widespread declines throughout California, a petition was submitted to the California Fish and Game Commission to list the burrowing owl as threatened under California’s Endangered Species Act [9]. Declines have usually been attributed to habitat loss and fragmentation, along with declines in fossorial mammal species that construct the burrows used by breeding burrowing owls [10].
Habitat fragments inclusive of fossorial mammals remained within Naval Air Station Lemoore (NASL) amid the intensively farmed landscape of Kings and Fresno Counties, California. NASL supported possible winter migrants from more northern populations and year-round resident breeders numbering 85 pairs in 1999 [11]. Consistent with other habitat fragments across the species’ range, conflicts arose between conservation objectives and emerging land-use objectives. To mitigate the impacts of emerging land-use objectives, which, at NASL, were to reduce Bird-Aircraft Strike Hazard and to install utility-scale solar energy facilities on the grassland portions of the airfield where burrowing owls occurred (Figure 1), the Navy proceeded to (1) eliminate ground squirrels and their burrows as a means to discourage burrowing owls, and, beginning in 2015, (2) to relocate burrowing owls to a 20 ha soil-capped landfill where artificial nest boxes were installed away from the airfield (US Fish and Wildlife Service 2017: https://www.fws.gov/story/2021-06/solving-unsolvable, last visited 29 August 2024). Because these measures typify mitigation implemented at other locations [9,12,13,14], we decided to assess the efficacies of each based on observational data we collected from NASL prior to the relocation effort.
To assess mitigation efficacy, it is essential to establish a baseline representation of the distribution and abundance of the population. Density is an efficient metric for this purpose because it is readily comparable to densities measured at other times and places so long as the density comparisons are scaled to the spatial areas from which they originated [15,16]. However, whereas density estimates typically represent the population during the breeding season, one of us found in another study that, where possible, resident burrowing owls shift locations during the non-breeding seasons, thereby requiring even more space than revealed by breeding-season density estimates [17] (K. S. Smallwood, unpubl. data). Habitat patches that do not provide sufficient space for such shifts might not suffice for long-term persistence due to exhaustion of food supplies needed during the breeding season or due to accumulation of parasite and predator loads at breeding sites [18].
On the other hand, density has itself been cited as a potentially limiting factor, where high densities might prove detrimental to the breeding population. Nearest-neighbor distance is a related metric to density that is often used to guide the installations of nest boxes to prevent crowding [12]. At one study site where the occupancy of nest boxes declined from eight to one within only 7 years of nest box installations, nearest-neighbor distances among the nest-box sites averaged half (84 m) those of nest sites constructed by ground squirrels [16]. However, it remained undetermined whether nest box occupancy declined due to crowding, deterioration of nest boxes, overgrown vegetation around the nest boxes, or over-isolation from ground squirrels and their alternative burrows and mutual predator alarm-calling.
A factor often cited as a limiter of spatial distribution is vegetation height, which, if too tall, is thought to interfere with the need for burrowing owls to surveil for predators [19,20,21]. Based on this hypothesized factor, a frequent conservation measure is to mow or graze vegetation or to relocate burrowing owls to areas of low-stature vegetation [12,19,22]. Another factor often cited as a limiter is the availability of protected nest cavities [22], so a frequent measure based on this factor is to construct nest boxes [9,13]. Nest box performance has been linked to nearness to California ground squirrels [23]—the species that constructs most of the nest cavities used by burrowing owls in this state. Burrowing owls have also been found to select nest sites amid the highest densities of ground squirrel burrow systems [16], which adds to the evidence that close proximity to ground squirrels brings more benefit to burrowing owls than just the availability of a nest burrow [23].
Surrounding land use is another potentially limiting factor, such as a preponderance of cropland over native grasslands, though a test of this hypothesis has suggested a more nuanced limitation, if any [24,25]. It could be that the effect of surrounding land uses such as cropland is mitigated by the size of the grassland patch in which burrowing owls select their nest sites, with more interior locations giving burrowing owls access to more of the grassland than is available to owls nesting closer to the edge.
Our objectives were to (1) estimate the size and numerical trend of burrowing owls at NASL and to interpret the numerical estimate by comparing it to density estimates from other study sites; (2) test whether burrowing owls shifted locations of non-breeding-season burrows and nest burrows in response to management actions that affected vegetation cover and the distribution and abundance of fossorial mammals in RMA 5; (3) test whether burrowing owls associated with interior or more peripheral aspects of habitat patches; and (4) assess the condition and use of nest boxes installed during 1997–2001, including examining the site fidelity of breeding-season and non-breeding-season burrowing owls and the spatial relationship between burrows used for breeding and those used for non-breeding-season refugia. Our study has direct application in the conservation of burrowing owls and the associated small mammal community throughout the species range.

2. Materials and Methods

We had the opportunity to survey for burrowing owls after the Navy contracted us to help conserve remnant populations of the endangered San Joaquin kangaroo rat (Dipodomys n. nitratoides). On the 43.1-ha RMA 5, we performed spring and fall surveys for San Joaquin kangaroo rats while also recording the locations of burrows used by burrowing owls, California ground squirrels (Otospermophilus beecheyi), and Botta’s pocket gophers (Thomomys bottae) from fall 2000 to fall 2013. Concurrently, we managed vegetation to benefit San Joaquin kangaroo rats, the results of which provided opportunities to test for numerical and breeding-site responses by burrowing owls. To help update the Burrowing Owl Adaptive Management Plan as part of NASL’s Resource Management Plan, we also performed surveys in all possible habitat areas on NASL in 2010 and 2013 while also assessing the conditions of 47 nest boxes that had been installed by contractors during 1997–2001. The nest boxes consisted of buried utility boxes connected via tubing to the ground surface, an elevated mound inclusive of wire mesh, and a short perch structure [26,27,28]. We also surveyed the entirety of the 833.7 ha mowed grassland portion of the airfield during both the winter and breeding seasons of 2013.

2.1. Study Area

NASL was a naval air station with permanent basing and homeporting of carrier-based tactical jet squadrons composed of 7602 ha within Kings (6372 ha) and Fresno (1230 ha) counties in the San Joaquin Valley, California. One of our study areas in 2012–2013 was the 1660 ha airfield. With two runways, it was surrounded by land managed in agricultural out-leases. Typical crops included cotton, winter wheat, tomatoes, alfalfa, safflower, and silage corn. Some fields were left fallow due to drought conditions. NASL included 1237 ha of known suitable burrowing owl habitat, and between 2003 and 2006, another 118.6 ha of agricultural leases was retired and allowed to revert to grassland immediately adjacent to the airfield (Table 1). Resource Management Areas (RMAs) 1 through 5 were interspersed across the northern portion of NASL and included special-status species, including burrowing owls (Table 1).
Another of our study areas was RMA 5, which we surveyed in 2001–2013. RMA 5 (including a portion of RMA 3) was 43.1 ha in size, located in the southwest quarter of Section 17, T18S, R19E (USGS 7.5′ quadrangle, “Vanguard, California”), at 67 m elevation. The soil was classified as Panoche clay loam, saline–alkali. The temperature averaged 17.2 °C (range: −10 to 46.1 °C) and precipitation averaged 19 cm (range: 8.6 to 41.7 cm) [29]. RMA 5 was surrounded by intensive agriculture, primarily cotton fields, but also tomatoes, safflower, and alfalfa (Figure 2). RMA 5 was used as a motocross track until 1992, when it was closed to public access because an unauthorized person destroyed kangaroo rat burrow systems while using a tractor to widen the track’s borders.
The vegetation in RMA 5 was consistent with California annual grassland series [30], composed primarily of non-native grasses such as red brome (Bromus madritensis rubens) and foxtail barley (Hordeum murinum), as well as a dominant stand of saltgrass (Distichlis spicata) on the southeast portion of the field. Because we needed to reduce thatch, open up space, and increase site productivity to conserve San Joaquin kangaroo rats in RMA 5, we experimentally cleared decadent vegetation in August and September 2001. We cut and raked vegetation >40 m from kangaroo rat burrows using a large agricultural tractor. Within 25–40 m from kangaroo rat burrows, we mowed and left chaff on the ground using a small tractor (Bobcat™, West Fargo, ND, USA) to minimize soil compaction and to maximize kangaroo rat maneuverability. Within 10–25 m from kangaroo rat burrows, we removed all vegetation using hand-held weed removers and handheld rakes. We performed a controlled burn on 15 May 2002, but 98% of RMA 5 burned because a fire break failed. We performed another burn in June 2005 and a third burn in June 2010, covering 82% of RMA 5.
A tall, dense stand of sweet clover (Melilotus indica) covered most of RMA 5 in 2005, and a tall, dense stand of annual atriplex (Atriplex argentea var. mohavensis) did the same in 2006. Few kangaroo rats survived these two years of tall, dense vegetation. Then, in 2007, drought reduced the number of new plants by 98.3% from the year prior, and the entire population of ground squirrels perished, likely due to starvation, by mid-May. This extreme drought persisted through 2009.
Airfield vegetation consisted of the same non-native species of bromes as occurred in RMA 5, but it was regularly mowed. Airfield grasslands were largely connected, but they were also fragmented by asphalt runways, taxiways, tarmacs and other facilities. California ground squirrels occupied airfield grasslands, but not contiguously. On the Navy’s behalf, USDA APHIS Wildlife Services used shooting and trapping in an effort to remove all birds from the airfield during 2013 (and perhaps earlier) and proceeded to eradicate ground squirrels from the airfield while we performed our burrowing owl surveys during winter 2012–13. Beginning in September 2013, the Navy disked the grassland around the approach end of Runway 32L, except for grassland within 32 m of 22 burrows occupied by non-breeding owls.

2.2. Nest Box Survey

During our surveys, we assessed the occupancy and condition of the installed nest boxes as we encountered them. Prior to our study, 41 nest boxes had been assessed for condition issues [22]. We located another 6 nest boxes, for a total of 47 in our assessment (Table 1).

2.3. Detection Surveys

Each April in 2001–2013, we spent 2–5 days measuring vegetation in RMA 5 while remaining attentive to the locations of burrowing owls. Each May and June, we returned to RMA 5 to locate and map burrows of San Joaquin kangaroo rats and burrowing owls on RMA 5. Using a pacing method to differentiate burrow systems based on surface soil such as soil mounds [31], we also mapped the centers of California ground squirrel and Botta’s pocket gopher burrow systems. We walked parallel transects spaced 12–15 m apart, often stopping to scan with binoculars for burrowing owls. Surveys began after dawn, usually ending by noon but sometimes extending through mid-afternoon. We used a Trimble Pathfinder Pro-XR and Trimble Geo-XT GPS (Trimble, Westminster, CO, USA) to map the locations of occupied nests of burrowing owls where we observed adult pairs, chicks, or adult males bearing faded plumage due to long-term solar exposure. Additional evidence of nesting attempts could include alarm calling, site tenacity when disturbed, decorations (e.g., plant debris, toad skins, bodies or parts of small mammals) at the burrow entrance, abundant shed feathers, whitewash, and pellets. We implemented the same methods at other sites within NAS Lemoore in 2003, 2005, 2010, and 2013 (Table 2), although we did not map the burrow systems of ground squirrels or pocket gophers at other sites except for RMA 4 in 2003, 13 ha of retired agricultural lease in 2010, 66 ha of the airfield in 2010, RMA 3, and RMAs 1 and 2 and the intervening pasture in 2010.
During the breeding season in 2013, we scanned the available habitat for burrowing owls on the airfield using 10×−15× binoculars from inside a parked vehicle at multiple roadside vantage points prior to pedestrian surveys. To avoid aircraft operations, we visited areas within 53 m of runways and taxiways before 0800 h and on weekends and holidays. We surveyed all areas until convinced we found all occupied nests. We also revisited occupied nests later in the season to verify breeding attempts persisting through the season.
Non-breeding-season surveys for burrowing owl burrows were also simultaneous with surveys for San Joaquin kangaroo rats. We surveyed for non-breeding-season burrows in fall (late September through October) in RMA 5 from 2000 to 2013 and in winter on the airfield from 10 December 2012 to 10 January 2013. We surveyed in teams of two, walking along the transect 20 m apart and frequently stopping to scan 360° for burrowing owls using binoculars. We examined all ground squirrel burrows for evidence of burrowing owl use. Evidence included flushed owls, whitewash, pellets, or shed feathers.
Although burrowing owls nest within cavities—usually fossorial mammal burrows—they usually also occupy a “nest site” composed of both the nest cavity and nearby accessory or satellite burrows [32] and a larger nesting territory [33,34]. Because fossorial mammal burrows often collapse or degrade within a few years, we measured the selection, abundance, and reuse of nest sites rather than specific burrows. Across 13 years of monitoring in RMA 5, and in 2010 and 2013 within a 66 ha overlapping survey area on the airfield, we examined reuse of nest sites by first identifying nest sites as occupied nests occurring within 10 m of each other between years. Because we did not track burrowing owl identities, we did not know whether nest sites were reused by the same or different individual burrowing owls.

2.4. Density, Distribution, and Nest Site Reuse

To interpret the number of breeding pairs of burrowing owls at NAS Lemoore, we compared numerical estimates of burrowing owls to the sizes of study areas used to make density estimates (Appendix A). We regressed log10 density on log10 study area size using linear regression analysis to account for the variation in density estimates due to study area size [16,35,36].
We used ArcView GIS to measure nearest-neighbor distances among nest sites on the airfield and RMA 5 during breeding and non-breeding seasons. For non-breeding-season burrows, we also measured the mean distance to the nearest nest site used in the previous breeding season in RMA 5 and the following breeding season on the airfield.
We measured the distance from each nest site to the field edge in RMAs 4 and 5. RMA 5 was completely surrounded by agricultural crops, whereas RMA 4 was adjacent to agricultural crops on three sides and on one side was separated from the airfield grassland by only a cyclone fence. We identified nest sites occurring ≤60 m (about 4 contiguous ground squirrel burrow systems) of the field perimeter, 60–120 m from the perimeter (“shallow interior”), and >120 m from the perimeter (“interior”). We used chi-square tests to test for disproportionate nest occurrences along the field edge, shallow interior, and interior. We related observed counts to expected counts as measures of effect, where an expected count was the total number of nests in the field multiplied by the ratio of the number of nests within the field’s edge, shallow interior or interior to the incidence (inc) of the field’s edge, shallow interior or interior. For example, if N = 10 nest sites were found in a field, but n = 5 were found in the interior, which composed inc = 0.2 (20%) of the area of the field, then E x p = N × i n c = 2 , and the observed number of nest sites in the interior numbers 2.5 times the expected number.

2.5. Vegetation Monitoring

We monitored vegetation from 2000 to 2013 in RMA 5. We established 21 stations systematically spaced about 150 m apart. Each spring, we placed pairs of square sampling frames of 0.305 × 0.305 m (0.093 m2) 0.3 m north and south of each station, and repeated these placements at 10 m intervals along a transect extending east for 5 pairs of samples per station. Within sampling frames, we either counted or estimated the individual ramets of every plant species identified, and we estimated the percent cover of bare ground, thatch, grasses, and herbaceous plants. We also measured the depth of thatch inside each corner of the sampling frame, where we also measured the vegetation height. We visually compared our annual measurements as means and symmetric 90% CIs, a few of which we truncated at 0, resulting in minor asymmetry.

3. Results

3.1. Breeding-Season Burrowing Owl Observations

From 1997 to 1999, NASL gained 33 nest sites [11], then lost 50 nest sites through 2013 (Figure 3). In 2000, 1 year following peak abundance, 13 pairs of burrowing owls occupied recently installed nest boxes, accounting for 19% of NASL’s breeding population. In 2013, 31 (84%) of NASL’s 37 pairs nested in natural burrows on the airfield, while 5 nested in retired agricultural land adjacent to the airfield and 1 pair nested on an embankment of solar evaporation ponds used for sewage treatment (Table 2). Since 1997, the airfield has included the largest number of nest sites at NASL, whereas RMA 5 has hosted the highest density of nest sites through 2007 (Table 2). The nest density (Y) among surveyed grasslands of NASL was about average relative to other published density estimates as an inverse power function of the study area’s size (X): log10(Y + 1) = 1.00 − 0.44 × log10 X (r2 = 0.68, p < 0.001) (Figure 4).
The number of nest sites in RMA 5 responded numerically to the 2001 vegetation removal treatments intended to benefit San Joaquin kangaroo rats, which preceded a rapid increase in ground squirrel abundance (Figure 5). The number of nest sites increased from an average of 5.4 pairs/year over the previous 5 years to 16 pairs in 2002. The number of nest sites declined in succeeding years to 0 in 2008, 2010, 2012 and 2013, and only 1 in 2011 after the ground squirrel population declined to zero during a severe drought.
Vegetation cover changed in response to management actions to recover San Joaquin kangaroo rats, but most especially in response to severe drought in 2007 (Figure 6). Vegetation conditions at sampling stations nearest the nest sites mirrored conditions averaged across RMA 5 in numbers of plants and percentages of grass and herbaceous cover, but the mean percent bare ground near nest sites averaged 67% of the RMA 5-wide mean, and the depth of thatch near occupied nests averaged 58% of the RMA 5-wide mean (Figure 6). Bromus diandrus contributed substantially to thatch, but we removed most of it mechanically or through burning until the 2007 drought, after which Bromus diandrus steadily increased in the absence of management (Figure 6C). Counts of Bromus diandrus ramets at vegetation-monitoring stations near nest sites averaged only 28% of the RMA 5-wide mean. Compared to mean counts of ramets across RMA 5, mean counts nearest the nest sites were only 3% for Melilotus indica and 7% for Distichlis spicata, but they were 165% for Vulpia bromoides and 147% for Amsinckia menziesii. Bromus diandrus, Melilotus indica, and Distichlis spicata grow in relatively tall, densely packed stands, whereas Vulpia bromoides and Amsinckia menziesii are generally shorter-statured and more sparsely distributed.
Nest sites were associated with higher densities of ground squirrel burrow systems. The densities of ground squirrel burrow systems averaged 43% higher (90% CI = 13% to 73% higher) within 60 m of nest sites compared to RMA 5-wide (Figure 7). The densities of kangaroo rat burrows within 60 m of nest sites were also greater than the densities of RMA 5-wide (Figure 7). The densities of pocket gopher burrow systems within 60 m of nest sites averaged lower than RMA 5-wide densities (Figure 7). Over 13 breeding seasons in RMA 5, the number of nest sites (Y) increased significantly with the increasing log10 number of ground squirrel burrow systems + 1 (X): Y = 0.0014 + 2.74X (r2 = 0.38, p < 0.05). The number of nest sites also increased significantly with the increasing number of kangaroo rat burrows (X): Y = 0.204 + 0.107X (r2 = 0.47, p < 0.05).
Burrows used by non-breeding burrowing owls in fall were also associated with higher densities of ground squirrel burrow systems. The densities of ground squirrel burrow systems averaged 43% higher (90% CI = 13% to 73% higher) within 60 m of burrowing owl burrows compared to the RMA 5-wide squirrel density (Figure 7). The densities of kangaroo rat burrows within 60 m of burrowing owl burrows were also greater than the densities of RMA 5-wide (Figure 7). The densities of pocket gopher burrow systems within 60 m of burrowing owl burrows averaged lower than the RMA 5-wide densities (Figure 7).

3.2. Position in the Field

Within RMA 4, we detected five nest sites in 2003, and all were >60 m from the field’s perimeter. The 55 nest sites we recorded in RMA 5 from 2001 to 2013 were associated significantly with the location in the field (χ2 = 15.25, d.f. = 2, p < 0.005), with nest sites occurring at distances of <60 m, 60–120 m, and >120 m to RMA 5’s perimeter 0.30 times, 1.44 times, and 1.36 times more than expected, respectively. The 103 non-breeding-season burrows in 2000 through 2013 were associated significantly with location in RMA 5 (χ2 = 21.04, d.f. = 2, p < 0.005), with occupied burrows occurring within <60 m, 60–120 m, and >120 m of RMA 5’s perimeter 0.40 times, 1.27 times, and 1.39 times more than expected, respectively. Through all years, nest sites <60 m from RMA 5’s perimeter numbered fewer than expected based on the sizes of the areas which were compared. Meanwhile, the ratio of the observed to the expected number of nest sites declined within 60–120 m of RMA 5’s perimeter and increased >120 m from RMA 5’s perimeter (Figure 8). The ratio of observed to expected non-breeding-season burrows declined <60 m from RMA 5’s perimeter and increased >120 m from RMA 5’s perimeter (Figure 8).

3.3. Burrow Spacing and Nest Site Reuse

Nearest-neighbor distances among nest sites in RMA 5 averaged 50% of the mean in RMA 4 and 25% of the mean across the airfield (Table 3). Variation (SD) in nearest-neighbor distances was related to study area size, as the smallest study areas contained single clusters of nest sites and the largest study area (airfield) contained scattered nest sites between four widely separated clusters of nest sites. Where we surveyed during fall and winter months, the mean nearest-neighbor distances were 32% to 72% of the distances between nest sites in the same fields during the breeding season, but the distances from the nearest nest sites the preceding spring were nearly the same as nearest-neighbor distances during the breeding season (Table 3).
We recorded 42 nest sites in RMA 5, of which 32 (76%) were used in 1 year, 8 (19%) were used in 2 years, 1 (2.4%) was used in 3 years, and 1 was used in 4 years. Years of burrow reuse did not associate strongly with any of our ground cover or ecological variables. Of the reused nest burrows, three were first used in 2001; four in 2002; and one each in 2003, 2005, and 2006. Seven were used 1 year later, two were used 2 years later, one was used 3 years later, two were used 4 years later, and one was used 6 years later. Reuse of the burrows spanned 2 years in four of the burrows, 3 years in two of the burrows, and 4, 5, 7, and 8 years in one burrow each.

3.4. Non-Breeding-Season Burrowing Owl Observations

Of the 162 non-breeding-season burrows that were occupied on the airfield in winter 2013, 158 (98%) were within raised squirrel complexes; that is, burrow entrances were above grade due to accumulation of excavated soil, thus indicating long-term use by ground squirrels. We found burrowing owls across all grassland areas of the airfield, but most occurred at the ends of runways, especially at the approach ends of 14 Left and 32 Left.
Eleven (7%) of the 162 winter burrow sites were subsequently occupied for nesting on the airfield; conversely, 65% of nest sites were not at burrow sites previously occupied in winter. Winter burrows on the airfield averaged 328 m from nest sites the following spring. Fall-occupied burrows in RMA 5, where less space was available for owls to select alternative burrow sites, averaged 95 m from nest burrows. We found no other obvious spatial correlation between winter and spring burrow sites across the airfield.
In winter, we detected 73 burrowing owls on the airfield, of which 71 occurred singly and 2 occurred together. At 72 burrows linked to observed owls, 5 (7%) showed no sign of use other than the owl’s detection, and 21 (29%) showed little wash. At 110 burrows where we found sign but no owls, 37 (34%) showed only little wash, although 8 of these also included one to a few pellets.

3.5. Nest Boxes

We checked the statuses of 47 nest boxes installed between 1997 and 2002. As far as we could determine, 6 nest boxes were installed in 1997 and another 19 were added prior to the 1999 breeding season. By 2001, at least 47 nest boxes had been installed. We believe 13 of these nest boxes were occupied by owls in 2000. However, we began encountering damaged and destroyed nest boxes as early as 2001. By April 2003, all 7 nest boxes in RMA 4 were severely damaged. Of 44 nest boxes checked by 2008, and despite repairs having been made to some, only 2 (4.5%) were in good shape and 6 (13.6%) were intact. We characterized these 6 nest boxes as intact in 2010 and 2013, whereas all 41 (87.2%) others were severely damaged, destroyed, or obliterated. Burrowing owls occupied none of the nest boxes we inspected in 2003, 2008, 2010 and 2013.

4. Discussion

NASL’s burrowing owl population was of regional significance, given that its 1999 breeding population composed 8.5% of the 1991–1993 numerical estimate across an 18,650 km2 sampling area in the lowland portion of California’s southern Central Valley [2]. However, NASL’s breeding population has declined since 1999, most notably in habitat areas outside the airfield. This decline was about 50% from 1999 through 2008, which was a more rapid decline than the estimated regional decline of 3.2% from 1991 through 2007 [8].
Possible contributing factors to the burrowing owl decline at NASL included cessation of vegetation management in RMAs, declines in ground squirrel abundance and prey abundance caused by drought, and the loss of nest site capacity that had been briefly generated artificially by the installation of at least 47 nest boxes. Many of the nest boxes had since been destroyed or badly damaged by Navy land use changes and animal burrowing, likely by coyotes (Canis latrans), feral dogs (Canis familiaris), American badgers (Taxidea taxus), and ground squirrels. Two of the nest boxes were obliterated by construction of a waste storage facility, and seven others were obliterated by discing of land that had been converted to agriculture. Some nest boxes outwardly appeared intact, and some were known to have been repaired after 2001, but all of these nest boxes were nevertheless vacant soon after installation, and all were certainly vacant from 2008 to 2013. We found a similar decline in occupancy of nest boxes installed at Dixon National Radio Transmission Facility [14], where the spacing between nest box sites averaged only 49 m, ground squirrels damaged entrance tubes, and tall, dense stands of plants grew over soil mounds overlying nest boxes.
While a common recommendation has been to maintain nest boxes to maintain use by burrowing owls [22,26,37,38,39], our finding of low nest site reuse, even in fossorial mammal burrows, suggests that burrowing owls naturally occupy particular nest sites only briefly. One study found that all 15 nest burrows checked in 1970–71 had been occupied by breeding burrowing owls in previous years, but this study included no supporting evidence of past occupancy [34]. Our next-year nest site reuse of 17% was toward the low end of reuse rates reported elsewhere: 12% [40], 20% [20], 43% [41], 46% [16], <50% [42], 52% [19], 55% [43] 60% [44], and 67% [45]. Longer-term nest site reuse lessens substantially, as burrowing owls reused only 1 (2.4%) of our 42 nest sites in RMA 5 over 4 years. At Dixon NRTF, we found 12% reuse over 6 years [16]. Next-year return rates have been higher to larger areas surrounding the nest site, such as 85% returning to burrows within 400 m of the nest site [46] and 90% returning to the same prairie dog town [20]. It has also been reported that pairs not returning to specific burrows used new burrows within 50 m of the previous year’s burrow [19]. These findings suggest natural, frequent shifting of nest sites, but higher reuse of nesting territories and colonies.
Given the growing evidence of naturally low nest site reuse, we question whether many well-maintained nest boxes would be occupied much longer than unmaintained nest boxes. A significant difference was found in the duration of nest box occupancy, with annually maintained nest box occupancy averaging 2.1 years and unmaintained nest box occupancy averaging 0.5 years [39]. However, even with maintenance, 26% of nest boxes were occupied in only 1 year, 5% were occupied in 4 years, and only one was occupied in 8 years. Occupancy rates have ranged 3% to 67% [26,37,47,48], but we note that long-term occupancy has been under-reported. At NASL, the well-intentioned installation of nest boxes might have generated a surplus of burrowing owls that subsequently struggled to find nesting opportunities, where by “surplus” we mean the number of adult burrowing owls potentially breeding in excess of the capacity provided by natural burrows. The surge of breeding pairs in RMA 5 the year following mechanical vegetation removal and a controlled burn likely reflected a potential surplus of burrowing owls produced from nest boxes installed one to four years earlier combined with improved habitat conditions in RMA 5, such as more ground squirrels and more burrows.
The abundance and distribution of ground squirrel burrow systems have been consequential to the abundance and distribution of burrowing owls during both the breeding and non-breeding seasons. By comparing ground squirrel burrow system densities within 60 m of occupied nests across RMA 5, we quantified disproportionate use by burrowing owls of high-density ground squirrel burrow systems. As the squirrel population increased, so did the disproportionate use of higher densities of squirrel burrow systems (Figure 7). While the squirrel population was on the increase during the early years of our study, burrowing owls disproportionately nested on portions of RMA 5 with higher densities of ground squirrels nearer the field’s edge, but as the squirrel population peaked in number and spatial extent, burrowing owls disproportionately nested within higher densities of ground squirrels in the field’s interior (Figure 8). Nest sites remained disproportionately within the field’s interior after the squirrel population crashed to zero, and these owls used the vacant burrows until a lack of maintenance by squirrels caused the burrows to collapse and disappear by 2010. Nest sites have often been located within the highest densities of burrows constructed by the local fossorial mammals [16,20,49,50,51,52]. It has been hypothesized that burrowing owls benefit from mutual alarm calling and the predator dilution effect of the local fossorial mammals [49]. Related to the pattern of nest attempts amidst higher burrow densities, an earlier study at NASL found that burrowing owls relocated after losing access to candidate satellite burrows within 20 m of the nest burrow [53].
Burrowing owls also attempted nesting within higher densities of San Joaquin kangaroo rat burrows, especially during the fall months when nest burrows were increasingly clustered within high-density portions of the increasing kangaroo rat population. Burrowing owls were, of course, not using burrows constructed by kangaroo rats because these burrows were too small, so if the relationship can be interpreted as functional, then it was likely one of predator and prey; otherwise, the relationship was coincidental.
During non-breeding seasons, burrowing owls were just as selective, if not more selective, of ecological conditions as during the breeding season. During non-breeding seasons, burrowing owls responded more to high-density clusters of kangaroo rats and ground squirrels, and they increasingly selected the field interior until 2009, when they occurred there nearly five times more than expected. As is perhaps of conservation significance, burrows occupied during the non-breeding season tended to be located far from nest sites of the same year. We hypothesize that this shifting of burrow locations between breeding and non-breeding seasons might be for the purpose of (1) seasonally resting food resources between areas of use, (2) entraining predators on burrows used during the non-breeding season that will be abandoned during the breeding season, (3) resting breeding areas to deplete parasite loads at nest sites, and (4) some combination of these factors (see [18] for similar hypotheses to explain the shifting-mosaic pattern of abundance among animal species). Whichever hypothesis might later remain unrefuted, it appears that the habitat area used during the non-breeding seasons expands on the habitat area used during the breeding season, and therefore contributes to the numerical capacity of breeding burrowing owls.
Within the sizes of fields we studied, nest densities appeared to be about average when compared to nest densities measured elsewhere in the species’ geographic range. Given the grassland areas at NASL, the densities we estimated translated to relatively large numbers of occupied nests, though not nearly as many as were recorded 210 km to the north-northwest in the Altamont Pass Wind Resource Area, California, in 2011 [36]. NASL could also have been strategically important to burrowing owls migrating long distances, as the vast majority of Kings County and the Central Valley portion of Fresno County has been converted to intensive agriculture. However, we observed a substantial numerical decline at NASL, which we attribute to discontinued management of annual grasslands for the benefit of wildlife, and to efforts on the airfield to eradicate ground squirrels and evict burrowing owls.
To eradicate ground squirrels on the airfield during the winter of 2012–2013, Wildlife Services injected gas into ground squirrel burrows, then ignited the gas to explode the burrow systems. Wildlife Services took these actions concurrently with our burrowing owl surveys, often in close proximity to us, but without coordinating with us. Wildlife Services assumed that burrowing owls would not occupy ground squirrel burrows lacking wash, pellets, or feathers (Nathan Lang, pers. comm. 2013). Our data indicate that this assumption was incorrect, because of the 72 burrows where we observed burrowing owls, 7% showed no sign of use other than the owl’s detection, and 29% showed little wash. We detected these owls only because we were looking for them, and some of them we saw by stopping our forward progress along transects to look behind us, seeing them as they relocated after we passed by their burrows. Even if Wildlife Services killed no burrowing owls during ground squirrel control, they destroyed nest sites, as 7% of the winter burrow sites were subsequently occupied for nesting on the airfield. The high-density nesting area at the approach end of Runway 32L was also disked since 2013, destroying the habitat around 12 occupied nests in 2013 and reducing the number of accessible winter burrows from 40 in 2013 (our data) to 6 in 2015 (Google Earth Pro V 7.3.2.5776, NASL, 36 17.793′ N, 119 56.306 W, eye altitude 3560 m, 20 May 2015). These practices, if continued, likely severely reduced the number of burrowing owl nest sites at NASL.

5. Conclusions

Conserving burrowing owls, which often involves mitigating the impacts of habitat loss, needs to incorporate several habitat elements that even the most well-designed, well-maintained nest box cannot provide alone. Burrowing owls in California select nest sites amongst the highest densities of ground squirrel burrow systems available, where alternate burrows are readily available and where owls likely benefit from mutual alarm calling and the predator dilution effect. Where possible, and where ground squirrels are in sufficient abundance, burrowing owls also select nest sites interior to the field, farther from road traffic and the operations of agricultural equipment. The translocation of burrowing owls outside areas desired for human activities should only be areas with sufficient numbers of ground squirrels, but it must be considered that if such places exist nearby, then they are likely already occupied by burrowing owls. Translocating burrowing owls to occupied habitat would likely be disruptive.
Candidate translocation sites should offer sufficiently deep, friable soils so that ground squirrels can excavate and maintain burrows. Inter-annual nest site reuse is naturally low, so a high capacity for nest site relocation appears important, along with ample interior space within a grassland patch sufficiently sized to support ≥12 pairs of adult owls >60 m from the patch edge. One dozen pairs is the smallest colony that, in our experience, persists longer than only a few generations. Furthermore, sufficient habitat space is needed to enable burrowing owls in the non-breeding seasons to occupy non-breeding-season burrows hundreds of meters from nest sites. In some locations, careful use of mowing and fire can maintain short-stature grasslands with plenty of bare ground and little to no thatch, thereby benefitting both ground squirrels and burrowing owls. Our study serves as an example of how an ecosystem approach, including conservation of the fossorial mammal species burrowing owls depend upon and maintaining sufficient space for owls to winter away from nest sites, more effectively conserves burrowing owls than does the provisioning of artificial nest boxes on diminishing fragments of habitat.

Author Contributions

Conceptualization, K.S.S.; methodology, K.S.S.; formal analysis, K.S.S.; investigation, K.S.S. and M.L.M.; data curation, K.S.S.; writing—original draft preparation, K.S.S.; writing—review and editing, M.L.M.; project administration, M.L.M. and K.S.S.; funding acquisition, M.L.M. and K.S.S. All authors have read and agreed to the published version of the manuscript.

Funding

The research specific to this study received funding from the U.S. Department of the Navy.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

Data supporting the reported results can be requested from the authors.

Acknowledgments

We thank the US Navy for funding and John Crane, Richard Rugen, Tim Schweitzer, and Melanie Colon for their logistical support as Navy employees. We thank Joanne Mount, Elizabeth Leyvas, Skye Standish, and Brian Karas for assistance with winter burrowing owl surveys and Erik Smallwood for help with a breeding season survey.

Conflicts of Interest

The authors declare no conflicts of interest.

Appendix A

Table A1. Sources of density estimates available for comparison to breeding pair density of burrowing owls at Naval Air Station Lemoore, California, 1999–2013, organized by publication year.
Table A1. Sources of density estimates available for comparison to breeding pair density of burrowing owls at Naval Air Station Lemoore, California, 1999–2013, organized by publication year.
SourcePlace
[54]Dahlia Drain and Greeson Slough, Imperial County, California
[55]Oakland Airport, California
[32]Albuquerque, New Mexico
[56]Idaho National Engineering Lab, Idaho
[57]Cape Coral, Lee County, Florida
[58]Ardath and Bounty, southcentral Saskatchewan
[43,59]Mapimi Biosphere Reserve, Durango, Mexico
[60]Snake River Plain, Idaho
[61]Rocky Mountain Arsenal, Colorado
[62]Fray Jorge National Park, Chile
[49]Western Nebraska
[63]University of California at Davis, California
[64]Badlands National Park, South Dakota
[44]Imagination Farms, Inc., Dade and Brower Counties, Florida
[65]Cape Coral, Lee County, Florida
[66]Shoreline Park and Moffett Field, Santa Clara County, California
[67]New Mexico State University
[68]Southwestern Dominican Republic
[30]Wall District, Buffalo Gap National Grassland, South Dakota
[69]Kirkland Air Force Base, Kirkland, New Mexico
[70]Custer and Prairie Counties, Montana
[71]Hanna, Alberta, Canada
[45]Naval Weapons Systems Training Facility, Boardman, Oregon
[46]South rim of Salton Sea, Imperial County, California
[50]Thunder Basin National Grassland, northeastern Wyoming
[72,73]Pantex Lake, Carson, County, Texas
[38,48]Mineta San Jose International Airport, California
[74]Imperial Valley, California
[75]Colonel Allensworth State Park, Tulare County, California
[4]Parkland and urban sites, south San Francisco Bay, California
[76]Vasco Caves Regional Preserve, Contra Costa County, California
[77]Lake Mead National Recreation Area and Marine Corps Air Ground Combat Center, California
[36]Altamont Pass Wind Resource Area, Alameda and Contra Costa Counties, California
[16]Dixon National Radio Transmission Facility, Solano County, California

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Figure 1. A family of burrowing owls on the airfield of Naval Air Station, Lemoore, California, 2013.
Figure 1. A family of burrowing owls on the airfield of Naval Air Station, Lemoore, California, 2013.
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Figure 2. Aerial view of Resource Management Area (RMA) 5, Naval Air Station Lemoore, where we monitored burrowing owls from 2000 to 2013. RMA 5 was nearly completely surrounded by annual field crops. Previously used motocross tracks are visible, as are vegetation and soil treatment plots. The 2006 image is from GobeXplorerTM.
Figure 2. Aerial view of Resource Management Area (RMA) 5, Naval Air Station Lemoore, where we monitored burrowing owls from 2000 to 2013. RMA 5 was nearly completely surrounded by annual field crops. Previously used motocross tracks are visible, as are vegetation and soil treatment plots. The 2006 image is from GobeXplorerTM.
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Figure 3. Trend of number of breeding pairs of burrowing owls observed on the airfield (squares and red lines) and across all habitat areas of Naval Air Station, Lemoore, California (circles and blue lines) 1997–2013.
Figure 3. Trend of number of breeding pairs of burrowing owls observed on the airfield (squares and red lines) and across all habitat areas of Naval Air Station, Lemoore, California (circles and blue lines) 1997–2013.
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Figure 4. Breeding pair density declines as an inverse power function with increasing study area size among published estimates from throughout the species’ geographic range. Solid circles denote density estimates where ≥1 pair was observed at NASL, solid diamonds represent fields in NASL where no burrowing owl pairs were observed, and dashed lines connect density estimates derived from sampling plots that were projected to larger study areas (large circles). The regression slope was estimated only from sampled study areas (small circles) where burrowing owls were observed.
Figure 4. Breeding pair density declines as an inverse power function with increasing study area size among published estimates from throughout the species’ geographic range. Solid circles denote density estimates where ≥1 pair was observed at NASL, solid diamonds represent fields in NASL where no burrowing owl pairs were observed, and dashed lines connect density estimates derived from sampling plots that were projected to larger study areas (large circles). The regression slope was estimated only from sampled study areas (small circles) where burrowing owls were observed.
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Figure 5. Counts of ground squirrel burrow systems 2000–2013 (A) and number of breeding pairs of burrowing owls 1997–2022 before [11] and during our study (B) in 43 ha RMA 5, Naval Air Station, Lemoore, California. Short dashed arrow indicates time of mechanical vegetation removal, solid arrows indicate controlled burns, and long dashed arrow indicates onset of severe drought.
Figure 5. Counts of ground squirrel burrow systems 2000–2013 (A) and number of breeding pairs of burrowing owls 1997–2022 before [11] and during our study (B) in 43 ha RMA 5, Naval Air Station, Lemoore, California. Short dashed arrow indicates time of mechanical vegetation removal, solid arrows indicate controlled burns, and long dashed arrow indicates onset of severe drought.
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Figure 6. Yearly mean percent bare ground (A), depth of thatch (B), counts of ripgut brome ramets (C), counts of all plant ramets (D), percent grass cover (E), and percent herbaceous plant cover (F) at all 21 monitoring stations (blue circles and lines) and stations closest to burrowing owl nest burrows (maroon squares and lines) in 2001–2013 in RMA 5, Naval Air Station, Lemoore, California, where the short dashed arrow denotes mechanical removals of vegetation, short solid arrows denote controlled burns, and long dashed arrow denotes the onset of a severe drought.
Figure 6. Yearly mean percent bare ground (A), depth of thatch (B), counts of ripgut brome ramets (C), counts of all plant ramets (D), percent grass cover (E), and percent herbaceous plant cover (F) at all 21 monitoring stations (blue circles and lines) and stations closest to burrowing owl nest burrows (maroon squares and lines) in 2001–2013 in RMA 5, Naval Air Station, Lemoore, California, where the short dashed arrow denotes mechanical removals of vegetation, short solid arrows denote controlled burns, and long dashed arrow denotes the onset of a severe drought.
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Figure 7. Annual mean burrow systems/ha within 60 m of burrowing owl nest burrows (left graphs) and non-breeding-season burrows (right graphs) regressed in RMA-5 wide burrow system density for ground squirrel (top graphs), San Joaquin kangaroo rat (middle graphs), and pocket gopher (bottom graphs) in 2000–2013, Naval Air Station, Lemoore, California. Dashed lines represent what would be equal densities between burrows counted within 60 m of burrowing owl burrows and within the entirety of RMA 5.
Figure 7. Annual mean burrow systems/ha within 60 m of burrowing owl nest burrows (left graphs) and non-breeding-season burrows (right graphs) regressed in RMA-5 wide burrow system density for ground squirrel (top graphs), San Joaquin kangaroo rat (middle graphs), and pocket gopher (bottom graphs) in 2000–2013, Naval Air Station, Lemoore, California. Dashed lines represent what would be equal densities between burrows counted within 60 m of burrowing owl burrows and within the entirety of RMA 5.
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Figure 8. Trends in association between breeding season (top graphs) and non-breeding season (bottom graphs) burrowing owl burrows with distance from the edge of RMA 5, Naval Air Station Lemoore, including the perimeter or shallow interior (left graphs) and the interior of the field (right graphs), where the dashed line at 1.0 represents no more burrows than expected.
Figure 8. Trends in association between breeding season (top graphs) and non-breeding season (bottom graphs) burrowing owl burrows with distance from the edge of RMA 5, Naval Air Station Lemoore, including the perimeter or shallow interior (left graphs) and the interior of the field (right graphs), where the dashed line at 1.0 represents no more burrows than expected.
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Table 1. Sites with potential or known burrowing owl habitat and numbers of nest boxes installed 1997–2001, Naval Air Station Lemoore, California.
Table 1. Sites with potential or known burrowing owl habitat and numbers of nest boxes installed 1997–2001, Naval Air Station Lemoore, California.
Study SiteHaManagementNest Boxes
Airfield833.7Regularly mowed annual grassland and volant wildlife actively abated15
Retired agriculture leases138.6Allowed to revert to grassland in 2003–2006; 118.6 ha mowed regularly and 20 ha unmanaged11
RMA 135.0Atriplex shrub and annual grassland1
Pasture between RMAs 1 & 250.6Grazed annual grassland0
RMA 240.5Wetland, annual grassland, and Eucalyptus grove1
RMA 34.2Flood basin; unmanaged shrubs and annual grasses0
RMA 442.2Unmanaged non-native annual grassland7
RMA 543.1Annual grassland that was burned, mowed, and cleared to conserve San Joaquin kangaroo rat0
Receiver site15.0Regularly mowed annual grassland0
Transmitter site23.3Regularly mowed annual grassland0
Landfill20.2Non-native annual grassland on 0.61-m soil cap, adjacent borrow pit10
Motocross area42.5Used by off-road recreational vehicles 0
Recreation area67.0Near base housing; annual grassland includes running path and other outdoor recreation facilities2
Sewage treatment ponds buffer20.4Regularly mowed annual grassland surrounding dirt levees lined on the inside with riprap0
Table 2. Burrowing owl breeding season survey results at Naval Air Station, Lemoore, California.
Table 2. Burrowing owl breeding season survey results at Naval Air Station, Lemoore, California.
Study SiteHaYearOccupied NestsOccupied Nests/km2
TotalSurveyed
Airfield, all grasslands833.7833.72013313.72
Airfield north of Runway 14L/32R833.766.02010710.61
Airfield north of Runway 14L/32R833.766.020131218.18
Retired ag lease adjacent Airfield138.628.22010310.64
Retired ag lease adjacent Airfield138.6123.4201354.05
RMA 1 35.035.0201025.71
RMA 135.035.0201300.00
Pasture between RMAs 1 & 250.650.6201000.00
Pasture between RMAs 1 & 250.650.6201300.00
RMA 240.540.5201000.00
RMA 240.540.5201300.00
RMA 34.24.2201300.00
RMA 4 (adjacent Airfield)42.242.22003511.60
RMA 4 a11.311.3201300.00
RMA 543.143.1200149.28
RMA 543.143.120021637.12
RMA 543.143.12003511.60
RMA 543.143.120041125.52
RMA 543.143.12005511.60
RMA 543.143.1200649.28
RMA 543.143.12007613.92
RMA 543.143.1200800.00
RMA 543.143.1200949.28
RMA 543.143.1201000.00
RMA 543.143.1201112.32
RMA 543.143.1201200.00
RMA 543.143.1201300.00
Receiver site15.015.0201000.00
Receiver site15.015.0201300.00
Transmitter site23.323.3201000.00
Transmitter site23.323.3201300.00
Landfill cap20.220.2200800.00
Landfill cap20.220.2201000.00
Landfill cap20.220.2201300.00
Motocross area42.542.5201300.00
Sewage ponds perimeter buffer20.420.42005314.71
Sewage ponds perimeter buffer20.420.4201314.90
a 30.9 ha subsumed to airfield in 2006.
Table 3. Nearest-neighbor distances among nest sites and burrows used during the fall and winter seasons and between fall/winter burrows and the nest sites of the same year, Naval Air Station, Lemoore, California.
Table 3. Nearest-neighbor distances among nest sites and burrows used during the fall and winter seasons and between fall/winter burrows and the nest sites of the same year, Naval Air Station, Lemoore, California.
SiteYear(s)HaNearest Neighbor Distance (m)
Nest SitesNon-Breeding-Season BurrowsNon-Breeding-Season Burrows to Same-Year Nest Sites
x ¯ SD x ¯ SD x ¯ SD
RMA 4200342.219090
RMA 52001–201343.1949768909597
Airfield, north aspect201066181121
Airfield, north aspect201366151138804314394
Airfield, all grasslands2013833.7369116611973328324
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Smallwood, K.S.; Morrison, M.L. Burrowing Owls Require Mutualist Species and Ample Interior Habitat Space. Diversity 2024, 16, 590. https://doi.org/10.3390/d16090590

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Smallwood KS, Morrison ML. Burrowing Owls Require Mutualist Species and Ample Interior Habitat Space. Diversity. 2024; 16(9):590. https://doi.org/10.3390/d16090590

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Smallwood, K. Shawn, and Michael L. Morrison. 2024. "Burrowing Owls Require Mutualist Species and Ample Interior Habitat Space" Diversity 16, no. 9: 590. https://doi.org/10.3390/d16090590

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