Burrows of desert tortoises (Gopherus agassizii) as thermal refugia for horned larks (Eremophila alpestris) in the Mojave Desert.
Abstract: The Mojave Desert is one of the driest and hottest deserts in North America. One would expect that birds living in this desert would be specialists adapted to survive such an environment. However, most of the avifauna present in the Mojave Desert range into cooler, more-humid regions. We report observations of horned larks (Eremophila alpestris) using burrows of the desert tortoise (Gopherus agassizii) during summer as refugia from hot above-ground temperatures. We show that horned larks appear selective of the micro-environment they choose and that burrows are the coolest, most humid, microsites available. By using burrows of desert tortoises, horned larks may reduce evaporative water loss by X65% and they may avoid physiological stress, or potentially death. Additional research should investigate the importance of burrows of desert tortoises to other species as it is likely to provide a key microhabitat to many species that reside in the Mojave Desert.

El desierto Mojave es uno de los mas secos y calientes en Norteamerica. Se pensaria que los pajaros que viven en este desierto son especialistas adaptados para soportar ese ambiente. Sin embargo, la mayoria de la avifauna del desierto Mojave tiene una distribucion geografica que se extiende a regiones mas frescas y humedas. Reportamos observaciones de alondras cornudas (Eremophila alpestris) usando madrigueras de tortugas del desierto (Gophems agassizii) durante el verano como refugio de las temperaturas altas en la superficie del suelo. Ensenamos que las alondras cornudas parecen discriminatorias del micro-ambiente que escogen, y que las madrigueras son los sitios mas frescos y humedos disponibles. Al utilizar las madrigueras de las tortugas del desierto, las alondras cornudas pueden reducir la perdida evaporatoria del agua hasta 65%, y pueden evitar estres fisiologico, o potencialmente la muerte. Investigacion adicional debe evaluar la importancia de las madrigueras de las tortugas del desierto para otras especies porque es probable que provean un micro-habitat a muchas especies que habitan en el desierto Mojave.
Subject: Desert tortoise (Environmental aspects)
Habitat (Ecology) (Environmental aspects)
Authors: Walde, Andrew D.
Walde, Angela M.
Delaney, David K.
Pater, Larry L.
Pub Date: 12/01/2009
Publication: Name: Southwestern Naturalist Publisher: Southwestern Association of Naturalists Audience: Academic Format: Magazine/Journal Subject: Biological sciences Copyright: COPYRIGHT 2009 Southwestern Association of Naturalists ISSN: 0038-4909
Issue: Date: Dec, 2009 Source Volume: 54 Source Issue: 4
Geographic: Geographic Scope: United States Geographic Name: Mojave Desert Geographic Code: 1USA United States
Accession Number: 216632279
Full Text: The horned lark (Eremophila alpestris) is a small (28-40 g), ground-dwelling, Holarctic species with isolated populations in Morocco and Colombia (Beason, 1995). Populations in North American are divided into 21 subspecies, which breed from the Arctic, south to Mexico, and are migratory in northern limits of their range and residents in the south. Their breeding range is limited by areas with suitable habitat characterized by open areas with sparse or short vegetation. Prairies, deserts, and agricultural areas represent typical habitats exhibiting these features. Geographic range of the species encompasses a wide range of temperatures from the freezing Arctic to desert heat. The desert horned lark (E. a. ammophilla) survives as a year-round resident of one the harshest climates in North America, the Mojave and Amargosa deserts (Beason, 1995). Little is known about how this subspecies copes with these environmental extremes.

The Mojave Desert is one of the hottest and driest regions in North America and is characterized by widely fluctuating temperatures both seasonally and diurnally (Rundel and Gibson, 1996). Availability of water is low, with annual precipitation of 5-12 cm/year (MacKay, 2003). In addition, daily low and high temperatures can fluctuate by as much as 25[degrees]C. During summer, midday temperatures often are >40[degrees]C and ground temperatures can approach 70[degrees]C, while in winter, temperature regularly drops below freezing (Rundel and Gibson, 1996). It is due to these conditions of extreme temperatures, low availability of water, and desiccating winds that desert animals exhibit an array of adaptations and behaviors to deal with thermoregulation. These may include behavioral, physiological, and morphological adaptations (Pough et al., 1996; Rundel and Gibson, 1996).

Many desert mammals, such as rodents, have adjusted their activity patterns to be crepuscular or nocturnal, thus, avoiding high daytime temperatures. However, it has been shown that most small birds are diurnal and, thus, have to cope with the more extreme aspects of the desert environment. It is generally believed that small birds are diurnal because they have higher body temperatures (41[degrees]C) than the ambient temperature and can withstand the desert heat (Rundel and Gibson, 1996). Birds are highly mobile and can fly great distances to reach water, unlike most other desert fauna. However, little is known about how the horned lark copes with ground temperatures reaching 70[degrees]C and air temperatures >40[degrees]C (Rundel and Gibson, 1996). There are few data regarding their activity patterns, except their use of shade cast from various structures during the hottest periods of the day (Beason, 1995). This species occupies a broad range of climatic variables, although subspecies from hotter regions have a narrower thermoneutral zone that peaks at ca. 35[degrees]C (Trost, 1972). Possible adaptations to desert life by horned larks include longer legs and a head with increased surface-to-volume ratio and reduced insulative cover to promote effective heat loss (Niles, 1973). Additionally desert subspecies exhibit paler coloration (Sibley, 2000), which may reduce solar absorption. While these adaptations may assist horned larks to live in a desert environment, it is behavioral adaptations such as selection of microhabitats that may further facilitate ability of this diurnal species to alleviate stresses of thermoregulation. In this paper, we report on horned larks using burrows of the desert tortoise (Gopherus agassizii) in the Mojave Desert. Data on temperature and humidity are presented to illustrate the importance of the burrow as a stable, cool, more-humid environment offering refuge from the extreme summer climate.

METHODS AND MATERIALS--Observations were made ca. 40 km NE Barstow, San Bernardino County, California, at 700-800 m elevation (Walde et al., 2007). The study area was on the United States Army National Training Center at Fort Irwin (35[degrees]N, 116[degrees]W). The study area was in an area that historically has received minor impacts from training and is now listed as critical habitat for the desert tortoise (United States Fish and Wildlife Service, 1994) and is protected from disturbance. The area is a gently sloping alluvial fan with a generally south-facing slope that is divided by several small washes and a few large ones. Vegetation is typical of the Mojave Desert and is dominated by creosotebush (Larrea tridentata) and white bursage (Ambrosia dumosa). Other perennials include Nevada jointfir (Ephedra nevadensis), desert allysum (Lepidium fremontii), silver cholla (Opuntia echinocarpa), goldenhead (Acamptopoppus sphaerocephalus), cheesebush (Hymenoclea salsola), and Mojave indigo bush (Psorothamnus arborescens). During May and june 2003, systematic transect surveys were conducted to find and locate desert tortoises. During these surveys, special effort was made to locate all burrows as desert tortoises regularly seek refuge within them. All burrows were labeled and Universal Transverse Mercator (UTM) coordinates were recorded with a Garmin 12 Global Positioning System (Garmin 12 Personal Navigator Unit, Garmin International, Olathe, Kansas). Additional research objectives into the behavior, movement patterns, and ecology of the desert tortoise required researchers to make regular visits to the study site. During June, July, and September, horned larks were observed in burrows of desert tortoises. When an observation was made, temperature of the air at 1 m above ground in the shade, temperature of the ground in full sun shaded by body, and temperature inside the burrow were recorded. Temperatures were measured within 10 min of observations using a Taylor Switchable Digital Pocket Thermometer (Taylor Precision Products, Oak Brook, Illinois) accurate to 0.1[degrees]C. In addition, we recorded physical characteristics of burrows, such as direction the burrow opened, if it was under a shrub, and if the burrow was located on a slope.

We gathered environmental data every 10 min in 2005 with five weather-station data loggers (Onset Computers, Bourne, Massachusetts) that were dispersed throughout the site and were set to record air temperature, relative humidity, and ground temperature. Air temperature and relative humidity were recorded with a temperature-relative-humidity smart sensor mounted 1 m above the ground in a solar-radiation shield. Hobo H8 temperature and relative humidity dataloggers (Onset Computers, Bourne, Massachusetts) were placed in open areas away from shrubs (n = 9), on the north side of large creosotebushes (n = 9), and in a series of burrows (n = 14). Some dataloggers malfunctioned and were replaced as soon as possible. Loss of an individual datalogger had little effect on results, as all variables for each dataset were averaged. The Hobo H8 in the open and ground temperature from the weather station were averaged to estimate true ground temperature. This is a reliable estimate when compared to hand-acquired data.

Results--We made four observations of horned larks using burrows of desert tortoises. The first observation was on 3 June 2003 at 1410 h PST, when we observed two fledgling horned larks standing ca. 20 cm inside the burrow being repeatedly fed by an adult bird. The burrow was on the northeast side of a creosotebush, near the base of a north-facing slope and the opening of the burrow faced 348[degrees]. The second observation was of a single horned lark on 11 July 2003 at 1050 h PST. This burrow was also at the northern edge of a creosotebush, on relatively flat terrain, and the opening of the burrow faced 310[degrees]. The third observation of a single bird was 5 days later on 16 July 2003 at 1055 h PST. This burrow was also on relatively flat terrain, but was not associated with a shrub, and the opening of the burrow faced 282[degrees]. The fourth observation occurred on 26 September 2003 at 1018 h PST. This observation was of two horned larks that were standing ca. 25 cm inside the burrow. This burrow was in a wash on the western side of a Nevada jointfir; the opening of the burrow faced 290[degrees].

Air, ground, and burrow temperatures taken at the time of the observations varied substantially by location, with temperatures in tortoise burrows representing the coolest microsite during our observations (Table 1). For illustrative purposes of what microhabitats were available for horned larks, sample data for temperature (Fig. 1) and relative humidity (Fig. 2) are presented showing the relationship between these values for the air at 1 m, open-ground temperature, shade of shrub, and inside the burrow for 15 June, 15 July, 13 August, and 15 September 2005.

DISCUSSION--The importance of burrows to desert tortoises is well illustrated by their use for multiple purposes, including loci of social interactions, nesting sites, hibernation sites, and for thermoregulation (Woodbury and Hardy, 1948; McGinnis and Voigt, 1971; Burge 1977, 1978; Hampton, 1981; Turner et al., 1984; Nagy and Medica, 1986; Bulova, 1994; Rostal et al., 1994; Zimmerman et al., 1994; Rautenstrauch et al., 1998; Duda et al., 2002). Burrows are essential to survival for desert tortoises in the Mojave Desert, as they provide shelter from lethal surface temperatures in summer, and typically maintain higher humidity, which aids in reduction of water loss (Zimmerman et al., 1994; Bulova, 2002). Surprisingly, little is known about the role this unique micro-environment may play in the life history, behavior, and ecology of other species.

Only 31 species have been documented to use burrows of desert tortoises, including two birds, the common poorwill (Phalaenoptilus nuttallii) and burrowing owl (Athene cunicularia; Luckenback, 1982). Our observation of burrows being used by horned larks adds a third species to this list. This list is in sharp contrast to the burrows of the gopher tortoise (Gopherus polyphemus) from the southeastern states, where >350 species have been documented using their burrow systems, of which >50 species are vertebrates (Jackson and Milstrey, 1989). Avian species documented to use burrows of the gopher tortoise include the northern bobwhite (Colinus virginianus), wild turkey (Meleagris gallopavo), Florida burrowing owl (Athene cunicularia floridana), Carolina wren (Thryothorus ludovicianus), American robin (Turdus migmtorius), Bachman's sparrow (Aimophila aestivalis), and eastern towhee (Pipilo erythrophthalmus, Jackson and Milstrey, 1989). Aside from the greater biological diversity in the Southeast compared to the Southwest, our explanation for the vast differences in documented associates in burrows between these two species of tortoise is that little research has been directed toward this topic. Certainly, associates in burrows would be expected within burrows of desert tortoises as they are one of the few places in the Mojave Desert during summer that have a favorable temperature for most species (Fig. 1), as was observed with the horned larks use of this micro-environment. Furthermore, in the arid desert, burrows are the most humid environments for most of the day (Fig. 2).

[FIGURE 1 OMITTED]

Although our observations are few, three of the four observations were made in burrows that were under shrubs. It is unknown what percentage of burrows of desert tortoises are under shrubs, although some researchers have suggested that shrubs are actively selected (Luckenbach, 1982; Berry and Turner, 1986; Wilson et al., 1999). Furthermore, all of the burrows had openings that were oriented in a westerly to northerly arc. Use of burrows under shrubs with opening toward the northwest could greatly affect microclimate of the burrow; specifically, one would expect it to be cooler than a burrow facing in a southerly arc that was not shaded by a shrub. Indeed, three of our observations were mid-morning and the burrows selected were in a west-to-northwest arc, which would have maximum shade at this time. Our one observation in the afternoon was in a burrow with a more northerly opening, which also would indicate selection of the greatest amount of shade at that time of day. Thus, horned larks seem to be choosing microsites and possibly direction of burrow openings, seemingly choosing those that are most thermally advantageous. It is unknown if desert tortoises purposely construct their burrows to face in a more northwestly direction; therefore, we cannot comment on whether the larks were simply using what was available to them.

Horned larks have a thermoneutral zone that extends to 35[degrees]C, although they reside in areas regularly above this zone (Fig. 1), which leads to increased metabolic rate and evaporative water loss (Trost, 1972). Water resources are not available to counter the high rate of evaporative water loss. Temperatures experienced by desert horned larks on the surface or in the shade of a shrub exceed the lethal thermal maxima of this species (Fig. 1; Trost, 1972). Therefore, to avoid potential death, extreme physiological stress, and use of precious resources, horned larks seek microsites that are below these temperatures. Air temperatures were cooler than ground temperatures in the shade (Fig. 1). This is likely due to the dappled nature of shade under large creosotebushes not being 100%, although it is representative of the shade available to avifauna. Therefore, as temperature in the air is somewhat cooler at some parts of the day, a bird could take shelter in a shrub; however, even in June air temperature is above the thermoneutral zone for >5 h of each day (Fig. la). It is only in September that air temperature does not exceed 35[degrees]C (Fig. Id), although ground temperatures are well above lethal limits. The only microsite that remained within the thermoneutral zone of the desert horned lark were burrows of the desert tortoise. These results are similar to observations for several species of larks that used burrows of lizards as thermal refugia during hot summer days in the Arabian Desert (Williams et al., 1999).

[FIGURE 2 OMITTED]

If desert horned larks remained above ground during our observations in June and July, they would have been exposed to air temperatures of ca. 40[degrees]C (Table 1; Figs. la and lb) and would have lost 0.932 g [H.sub.2]O [h.sup.-1], or 3.6% of their body mass/h based on values adapted from Trost (1972). Obviously, this high rate of evaporative water loss is unsustainable, especially in the Mojave Desert where little free water is available. By seeking shelter in burrows of desert tortoises, horned larks exploit a microclimate within its thermoneutral zone during June-September, and they reduce evaporative water loss to 0.325 g [H.sub.2]O [h.sup.-1], or 1.25% of their body mass/h (Trost, 1972). Thus, they could have reduced their evaporative water loss by ca. 65% by seeking shelter in a burrow of the desert tortoise. This does not consider that burrows of desert tortoises are the most humid diurnal microclimate, which could further reduce water loss (Fig. 2). Similar results have been observed for other desert-dwelling birds (Trost, 1972; Wolf and Walberg, 1996; Williams et al., 1999). Survival of these birds in desert environments depends on finding a suitable microclimate within their tolerable limits (Wolf et al., 1996; Williams et al., 1999; this study).

Diversity of birds in the Mojave Desert is likely regulated by daily temperatures >35[degrees]C for extended periods of time and regular shaded air temperatures >45[degrees]C. If birds are not able to minimize evaporative water loss through selection of microsites, as observed by Wolf et al. (1996) and in our study, it would certainly result in death. Other microsites, such as deep shade provided by large rocks, or walls of desert washes, may also provide suitable microsites. However, shaded sites are less thermally buffered than burrows of desert tortoises (Fig. 1), and will, therefore, result in increased metabolic rates and evaporative water loss. Trost (1972) showed that evaporative water loss for horned larks increased rapidly >35[degrees]C. Temperatures in burrows, while inside the thermoneutral zone of horned larks, were close to the 35[degrees]C upper limits of the thermoneutral zone during July and August (Figs. 1b and 1c). As such, global climate change could have a negative effect on bird life in the Mojave Desert and other deserts, if birds are not capable of finding suitable microsites where they can moderate evaporative water loss. Populations of desert tortoises have been declining for decades; thus, the number of unique microsites that they create in the Mojave Desert also is likely to be declining. Additional research should investigate the importance of burrows of desert tortoises to other species, as it is likely to provide a significant microhabitat to many species that reside in the Mojave Desert.

We acknowledge the United States Army Construction Engineering Research Laboratory for initiating and funding the project. M. Quillman from Department of Public Works Environmental at the National Training Center, Fort IrMn, California, contributed logistical support and funding. In addition, this project could not have been completed without the numerous field hours contributed by our dedicated staff. Research on the desert tortoise was conducted under recovery permit TE066452-1 issued by the United States Fish and Wildlife Service and Memorandum of Understanding for Scientific Collecting Permit 802005-03 issued by California Department of Fish and Game.

Submitted 9 October 2007. Accepted 15 May 2009.

Associate Editor was Michael S. Husah.

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ANDREW D. WALDE, * ANGELA M. WALDE, DAVID K. DELANEY, AND LARRY L. PATER

ITS Corporation, 8000 San Gregorio Road, Atascadero, CA 93422 (ADW)

Walde Research & Environmental Consulting, 12127 Mall Boulevard, Suite A156, Victorville, CA 92392 (AMW)

United States Army Construction Engineering Research Laboratory, P.O. Box 9005, Champaign, IL 61826 (DKD, LLP)

* Correspondent: amalde@hotmail.com
TABLE 1--Temperatures ([degrees]C) of air (1 m above ground in
shade), ground (in full sun shaded by body), and inside burrow of
the desert tortoise (Gapheras agassizii) at the time burrows were
used by horned larks (Eremophila alpestris) as refugia in the
study area ca. 40 km NE Barstow, San Bernardino County,
California.

Observation   Air    Ground   Burrow

1             40.5    57.4     32.0
2             39.5    53.2     32.8
3             39.9    49.5     34.0
4             31.0    40.3     22.6
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