Burrowing Owls (Athene cunicularia) were once common breeders in grasslands throughout North America. Abundance of Burrowing Owls has declined sharply in Canada and the species is listed as endangered under the Canadian Species at Risk Act (Committee on the Status of Endangered Wildlife in Canada [COSEWIC] 2006). The population trajectory of Burrowing Owls in the US has been less clear and has been a topic of debate for decades (Haug et al. 1993, Sheffield 1997, Klute et al. 2003, Poulin et al. 2011). Burrowing Owls are listed as a Species of National Conservation Concern in the US and in every US Fish and Wildlife Service Region in which they occur (US Fish and Wildlife Service 2008), and have experienced population declines in at least some portions of their US breeding range (Smith et al. 1997, Dechant et al. 1999, Desmond et al. 2000, Wellicome and Holroyd 2001, Klute et al. 2003, Conway and Pardieck 2006, DeSante et al. 2007, but see DeSante et al. 2004, Bartok and Conway 2010). Moreover, Burrowing Owls are listed as endangered, threatened, or a species of concern in nine states (Klute et al. 2003) and several articles have documented a contraction in the spatial extent of their breeding range (Wellicome and Holroyd 2001, Macías-Duarte and Conway 2015). However, we lack a thorough examination of the available data regarding population trends of Burrowing Owls (especially in the US) and how those trends vary spatially across the species' range. To address this need, I aimed to use data from the North American Breeding Bird Survey program (Ziolkowski et al. 2010) to examine the temporal and spatial patterns in Burrowing Owl population trends during the past 60 yr.

Documenting population trajectories of imperiled species is useful, but such information, alone, does not provide guidance on causes of declines or management actions that may help reverse declines. Many potential factors have been mentioned as causes of population declines in Burrowing Owls, but reductions in numbers of burrowing mammals is often included as one of the likely causes (Zarn 1974, Desmond and Savidge 1996, Sheffield 1997, Desmond et al. 2000, Conway et al. 2006, Conway and Pardieck 2006, Poulin et al. 2011). Burrows are a critical resource for Western Burrowing Owls (A. cunicularia hypugaea; Coulombe 1971, Zarn 1974) because they do not dig burrows themselves; they depend on the abandoned burrows of burrowing animals (in contrast, Florida Burrowing Owls, A. cunicularia floridana, dig their own burrows). Hence, persistence of the burrowing animals that dig the burrows on which Western Burrowing Owls depend likely influences population trends and persistence of the owls. Yet, no current literature summarizes the relative importance of the different burrowing species on which Western Burrowing Owls depend throughout their breeding range. To fill this data gap, I aimed to create the first summary of the symbiotic relationship between Western Burrowing Owls and the suite of species of burrowing animals on which they depend throughout their breeding range. I used range maps of burrowing animals in North America to develop a map that depicts the primary burrowing species on which Western Burrowing Owls depend throughout their range, and I consulted the Burrowing Owl literature to validate the map. This map (and future revisions of it) should provide a more informed discussion of the importance of revised policies for managing the burrowing animals upon which Western Burrowing Owls depend. I then used this map to examine whether population trends of Western Burrowing Owls differed among portions of the owl's breeding range where they rely on different species of burrowing animals.

Methods

Results

Burrowing Owls in Canada have declined dramatically over the past 50 yr (6.0–13.5% annual rate of decline) and the BBS trend estimates for Canada have been significant since at least 1998 (Table 1). In contrast, the estimates of long-term population trends for Burrowing Owls in the US reported by the BBS program were negative but not deemed statistically significant from 1999–2010 despite the fact that the point estimate suggested a decline of −0.7% to −2.2% annually since 1999 (Table 1). The long-term trend estimate for Burrowing Owls in the US was significant for the first time in 2011 (i.e., the confidence interval for the trend no longer overlapped zero in the years 2011–2015; Table 1). However, population declines in the US are most apparent prior to 1995; the average number of Burrowing Owls detected per occupied BBS route declined from 0.80–1.40 owls per route during 1966–1983 to 0.20–0.70 owls per route during 1995–2014 (for the 168 routes that were initiated prior to 1970; Fig. 1).

Table 1. 

Estimates of population trend for Burrowing Owls in the US and Canada from the North American Breeding Bird Survey Program.

Figure 1. 

The average number of Burrowing Owls detected per BBS route per year (for the routes that detected ≥1 Burrowing Owl during ≥1 yr) based on the 168 BBS routes in the US that were initially surveyed prior to 1970. Error bars indicate ± 1 SE.

When I examined the proportion of BBS routes with negative slopes, Burrowing Owls in the US seem more clearly to be declining (compared to inferences from an overall linear trend). More BBS routes in the US with Burrowing Owls had a negative slope than a positive one (χ² = 14.53, df = 1, P <0.001): 257 BBS routes had positive slopes (42%), 351 BBS routes had negative slopes (57%), and 4 routes had slopes of zero. In comparison, 9 BBS routes had positive slopes (31%) and 20 BBS routes had negative slopes (69%) in Canada (χ² = 4.17, df = 1, P = 0.041). The percentage of BBS routes that had negative slopes varied nonlinearly with latitude, but not longitude (Table 2, Fig. 2).

Table 2. 

Relationship between Burrowing Owl population trajectory (increasing or decreasing) and latitude and longitude based on binary logistic regression of survey data from 1966–2015 along 612 BBS routes in the US. The quadratic term for latitude (latitude²) was significant, indicating a significant nonlinear relationship between population trajectory and latitude. β is the beta coefficient from a binary logistic regression and Wald is the test statistic describing how the coefficient differs from zero.

Figure 2. 

The relationship between latitude and the percent of BBS routes with negative trends (1966–2015) for 612 BBS routes in the US. To illustrate the relationship, the 612 routes were split into 10 latitudinal bins with equal numbers of BBS routes. The numbers on the x-axis are the mid-points of those 10 latitudinal bins.

Western Burrowing Owls primarily use black-tailed prairie dog burrows in the eastern portion of their breeding range, whereas the diversity of burrowing species on which they depend is much greater in the northern and central portions of their breeding range (Fig. 3). Most (90%) of the study locations from published articles that mentioned the primary type of nest burrow used by Western Burrowing Owls corroborated the primary burrow usage map. The primary burrow type used by Western Burrowing Owls differed from the one predicted on the map at only 8 of the 81 study sites in past studies (the orange squares in Fig. 3). Five of the eight incongruities were in New Mexico. Based on the burrow usage map, four species of burrowing mammals are the primary burrow provider within 61% of the Western Burrowing Owl's range: black-tailed prairie dog (35% of its range), yellow-bellied marmot (11%), Richardson's ground squirrel (10%), and American badger (26% of its range, including areas where badgers are considered co-primary burrow providers along with marmots and Richardson's ground squirrels). Other burrow providers are important in more localized areas: round-tailed ground squirrel (6% of the owl's range), rock squirrel (6% of the owl's range), Gunnison's prairie dog (5% of owl's range), California ground squirrel (5% of owl's range), and seven other species that were the primary burrow provider in <5% of Western Burrowing Owl's range (Fig 3).

Figure 3. 

The Western Burrowing Owl uses abandoned burrows dug by burrowing animals for its nest burrow and the primary architect of the owl's nest burrows differs throughout the owl's breeding range in North America. The map is based on the overlap in the distribution of Western Burrowing Owls and the distributions of the burrowing animals that dig the burrows that the owls primarily use. White areas on the map indicate areas outside the Western Burrowing Owl's range and the hatched areas indicate portions of the owl's historical range where it no longer occurs (based on Wellicome and Holroyd 2001). The different colors represent the assumed species of burrowing animal on which the Western Burrowing (Figure caption continued on the bottom of the next page.) Owl primarily relies in that portion of its range (see text for rationale). The numbered symbols are the locations of studies that have reported the primary type of burrow used by nesting Western Burrowing Owls and whether the study corroborated (green circle) or did not corroborate (orange square) the assumptions of the map: (1) Haug 1985; (2) James et al. 1990; (3) Scobie 2015; (4) Wellicome et al. 1997; (5) Warnock and Skeel 2002; (6) Stewart 1975, Murphy et al. 2001; (7) Dominguez 2010; (8) Grant 1965; (9) Davies and Restani 2006; (10) Conway et al. 2006; (11) Climpson 1977; (12) Konrad and Gilmer 1984; (13) Restani et al. 2001; (14) Conway et al. 2006, Smith and Conway 2007, 2011; (15) Holmes et al. 2003; (16) Green and Anthony 1989; (17) Conway and Simon 2003; (18) Griebel 2000, Griebel and Savidge 2007; (19) MacCracken et al. 1985; (20) C. Conway unpubl. data, Conway and Simon 2003; (21) Martell et al. 1993; (22) Gleason 1978, Gleason and Johnson 1985; (23) Brady 2004, King and Belthoff 2001; (24) Belthoff et al. 1995; (25) Conway et al. 2005, Lantz et al. 2007, Lantz and Conway 2009; (26) Rich 1986; (27) Brady 2004; (28) Rich 1984; (29) Desmond et al. 2000; (30) C. Lundblad pers. comm.; (31) Conrey 2010; (32) Hughes 1993; (33) Smith and Murphy 1973; (34) Plumpton and Lutz 1993, Plumpton 1992; (35) Neel 1999; (36) Johnson 1997; (37) C. Conway unpubl. data; (38) Thomsen 1971; (39) Trulio 1997; (40) Hall et al. 2003, Steen et al. 1997, Greger and Hall 2009; (41) Butts 1972, Butts and Lewis 1982; (42) Gervais 2002, Gervais et al. 2003; (43) Ray et al. 2016, Teaschner 2005; (44) Bayless and Beier 2011; (45) Ronan 2002, Ronan and Rosenberg 2014; (46) Arrowood et al. 2001, Martin 1973; (47) Hawks Aloft 2003; (48) Ross 1974; (49) Berardelli et al. 2010; (50) Rosenberg and Haley 2004, Catlin 2004, Bartok and Conway 2010; (51) Unitt 2004; (52) Conway et al. 2007, Ogonowski and Conway 2009; (53) Johnson et al. 1997; (54) Itubarría-Rojas 2002; (55) Ogonowski and Conway 2009, Conway and Ogonowski 2005; (56) Best 1969; (57) A. Macías-Duarte pers. comm.; (58) Russell and Monson 1998; (59) Dominguez 2010, McNicoll 2005; (60) Macías-Duarte 2011; (61) Rodriguez-Estrella and Ortega-Rubio 1993; (62) Ruiz Ayma et al. 2016.

The percent of BBS routes with negative population trends was highest in portions of the owl's range where the primary burrow provider was Richardson's ground squirrel, California ground squirrel, black-tailed prairie dog, and American badger (Table 3, Fig. 3). These regions were in the northernmost, westernmost, and easternmost portions of the Western Burrowing Owl's range.

Table 3. 

Percent of BBS routes with a negative trend (1966–2015) within portions of the Burrowing Owl's range that differ based on the primary burrower provider (i.e., the polygons in Fig. 3).

Discussion

Population trend estimates from the BBS program suggested nonsignificant trends for Burrowing Owls in the US for many years. The BBS program changed analytical methods in 2011 and the long-term trends for Burrowing Owls in the US were significantly negative for the first time in 2011. Most of the declines in Burrowing Owl abundance occurred in the 1970s, 1980s, and early 1990s, but the analytical methods used prior to 2011 did not detect a significant decline. However, population declines of the magnitude suggested by the point estimates even in years prior to 2011 (−0.7% to −2.2% annually) are substantial even though they are likely underestimates of the rates of decline and were not statistically significant. A 1% annual decline in abundance over a 49-yr period (e.g., 1966–2015) equates to a 39% decline in abundance over those 49 yr. Low relative abundance of Burrowing Owls likely affected the statistical power of the trend estimates from the earlier analytical method. Indeed, numerous local and regional studies have documented population declines of Burrowing Owls (Desmond et al. 2000, Klute et al. 2003, Conway and Pardieck 2006).

Our methods did not control for changes in BBS surveyors over time. Failure to include observer as a covariate when estimating linear trends in BBS counts usually results in a positive bias in trend estimates (Sauer et al. 1994), so the higher proportion of negative trends on BBS routes is likely real and may actually be higher than what is reported here. Why have Burrowing Owls at the northernmost and southernmost portions of their US breeding range declined more than owls in the central portion of their US range? One hypothesis is that there are fewer burrow excavators at these latitudes. For example, perhaps the abundance and distribution of Richardson's ground squirrels, American badgers, and black-tailed prairie dogs have declined more so than other burrowing animals on which Burrowing Owls depend in the central portion of their US range (Fig. 3). Indeed, burrow availability is considered a primary habitat feature in the northern portions of the owl's range (Uhmann et al. 2001, Lantz et al. 2007) and the owl's population trends were more likely to be negative in portions of their range where they rely on these three species compared to other portions of their range (Table 3). Robust estimates of the extent of population declines among the different species of burrowing animals are needed to more rigorously test this hypothesis, but such estimates are currently lacking. Abundance of American badgers has declined, especially in the northern part of their range and in portions of their range where prairie dogs were formerly more abundant (Reid and Helgen 2008), and marmots are frequently removed by landowners in the northern portions of the US (C. Conway unpubl. data). Alternatively, the higher rates of decline in the northernmost portion of the owl's range may not be related to latitudinal variation in the types of burrows used, but rather may reflect differential changes in migratory behavior for owls in northern latitudes (Macías-Duarte 2011, Macías-Duarte and Conway 2015) or differences in farming practices, urbanization, or the differential effects of climatic changes (e.g., drought) or sylvatic plague at different latitudes. Indeed, Burrowing Owls have substantial intraspecific variation in reproductive traits (Conway et al. 2012) and latitudinal variation in these traits may contribute to the latitudinal variation in population trend (and provide clues to its underlying cause).

BBS routes are roadside surveys, so the trend estimates derived from BBS count data represent population trends of Burrowing Owls near roads. This is less likely to bias trend estimates of Burrowing Owls compared to similar approaches based on data for other bird species because Burrowing Owls do not seem to avoid roads. Indeed, daytime space use by owls in Canada showed they preferred fences (which are often along roads) and gravel and dirt roads, but avoided paved roads with high-speed traffic (Scobie et al. 2014). Additionally, owls seem to preferentially nest and forage near roads in at least some portions of their range (Haug et al. 1993, Conway and Pardieck 2006, Poulin et al. 2011). Another bias associated with trend estimates from BBS count data (or any count data) is the first-time effect; an observer's skill level increases after his or her first year of surveys (Kendall et al. 1996). The first-time effect is likely small for Burrowing Owls compared to other birds for the reasons mentioned above, and it causes trend estimates to be positively biased (Kendall et al. 1996), so the rate of decline may be even greater if the first-time effect influences Burrowing Owl counts on BBS routes. Some of the biases associated with trend estimates from BBS counts could be ameliorated if range-wide surveys designed specifically for Burrowing Owls were conducted (Holroyd and Wellicome 1997, Conway and Simon 2003, Conway et al. 2008).

Western Burrowing Owls rely on burrows dug by burrowing animals for nesting, roosting, and escape from predators and thermal extremes. Western Burrowing Owls modify and expand existing burrows, but they rarely initiate new burrows. Hence, burrowing animals are a critical resource for Western Burrowing Owls, and the fate and protection of the burrowing animals that dig the burrows on which owls depend likely influence population trends and persistence of Western Burrowing Owls (Wellicome and Holroyd 2001). As such, preservation of colonial burrowing animals is often one of the most common recommendations regarding methods to help conserve Burrowing Owls (Zarn 1974, Holroyd et al. 2001). The map presented here is the first effort to summarize and map the primary burrow types used by Western Burrowing Owls throughout their breeding range in North America. The map proved to be quite accurate when validated against 81 studies that reported the primary type of burrow used by nesting Western Burrowing Owls. The one area where the map did not perform well was New Mexico: five of the six Burrowing Owl studies in New Mexico were conducted within the IUCN range of black-tailed prairie dogs but they reported that owls primarily rely on a species other than black-tailed prairie dogs. This lack of congruence in New Mexico could reflect: (1) a lack of precision in the IUCN range maps in New Mexico, or (2) that black-tailed prairie dogs may have been eradicated in areas where Western Burrowing Owl studies have been conducted in New Mexico. For example, several studies in New Mexico reported that Western Burrowing Owls used rock squirrel, badger, or kangaroo rat burrows and that prairie dogs were not present in their area (despite being within the IUCN range).

With the exception of New Mexico, 67 of the 68 Western Burrowing Owl studies in the US and Canada corroborated the assumptions in the burrow usage map. I was not able to adequately validate the map in several portions of the Western Burrowing Owl range because I was unable to find studies in those areas that mentioned the primary burrow provider. I recommend that investigators who work in the following areas record the primary burrow provider to help further validate the map: Mexico, Nevada, northern Arizona, and southern Utah. The map suggests that conservation of black-tailed prairie dogs, American badgers, California ground squirrels, and round-tailed ground squirrels may be particularly important to the conservation and persistence of Western Burrowing Owls, as these four species are the primary burrow providers in the majority of the owl's range in the US and Canada. A broad-scale map like this cannot be 100% accurate in every location in North America because Western Burrowing Owls use a variety of burrow types in most portions of their range. For example, Burrowing Owls will also use the burrows of skunk, fox, coyote (Canis latrans), armadillo, other ground squirrel species (Townsend's [Urocitellus townsendii], etc.), and other burrowing animals not depicted on the map. Hence, this map is a simplified depiction of the burrowers that are important to Western Burrowing Owls, and conservationists or managers should not assume that, for a given area, only the species depicted in this map is important for Western Burrowing Owls. Indeed, in some instances, the primary burrow type may be in such low abundance that it is not the most commonly used burrow type. Despite these caveats, this map will provide a template for future refinement regarding the primary burrow providers for Western Burrowing Owls, and this map and future refinements of it will promote analyses regarding whether spatial patterns in declines in Western Burrowing Owl abundance are related to the burrowing species that dig the burrows on which they depend. This map can also be used to assess whether demographic traits and population viability vary among regions based on the primary burrowing species that provides burrows for Western Burrowing Owls. As such, this map may help future investigators generate and test hypotheses regarding the most likely cause(s) of observed population declines in Western Burrowing Owls.

What are the characteristics of underground burrows that make those created by one burrowing species more preferable to Western Burrowing Owls compared to those of another species? Diameter, depth, slope, number of turns, number of entrances, soil associations, longevity, and distance between adjacent burrows are some of the many burrow characteristics that likely vary among burrow providers and many of these traits affect use by Western Burrowing Owls (Belthoff and King 2002). Indeed, Western Burrowing Owls show preferences for some of these features (Smith and Belthoff 2001), but more research is needed to quantify how the burrows created by the different burrowing species differ from what Western Burrowing Owls prefer. Of the suite of burrowing animals that create burrows that are subsequently used by Western Burrowing Owls, some are likely more important to the conservation of owls than others. Some of the species depicted in the burrow usage map (Fig. 3) have experienced substantial declines in abundance and distribution (e.g., black-tailed prairie dogs, and American badgers). Other species have likely fared much better over the past century (e.g., round-tailed ground squirrels, white-tailed prairie dogs, and rock squirrels). Most Burrowing Owl publications do not state what species created the burrows used by owls in their study site. Those that do, often only state the primary species, and the few that describe all burrow types used by owls rarely state the proportions for each burrow type used or even rank their relative importance. This is surprising given the importance of burrowing animals to Western Burrowing Owls. I urge future authors to document and report the burrow types used by Western Burrowing Owls in their study area, so that more detailed versions of the map included here are possible. For example, future revisions of the burrower provider map should include “secondary” and “tertiary” species of burrowers used by owls in each portion of their range so that the map can better inform Western Burrowing Owl conservation efforts.