Journal of Threatened Taxa |
www.threatenedtaxa.org | 26 August 2023 | 15(8): 23662–23668
ISSN 0974-7907
(Online) | ISSN 0974-7893 (Print)
https://doi.org/10.11609/jott.8435.15.8.23662-23668
#8435 | Received 11
March 2023 | Final received 10 July 2023 | Finally accepted 08 August 2023
Observations of Gray Fox Urocyon cinereoargenteus
(Schreber, 1775) (Mammalia: Carnivora: Canidae)
denning behavior in New Hampshire, USA
Maximilian L. Allen 1 & Jacob P. Kritzer
2
1 Illinois Natural History Survey,
University of Illinois, 1816 S. Oak Street, Champaign, IL 61820, USA.
2 Northeastern Regional Association
of Coastal Ocean Observing Systems, 195 New Hampshire Avenue #240, Portsmouth, NH
03801, USA.
1 maxallen@illinois.edu
(corresponding author), 2 jake@neracoos.org
Editor: H.N. Kumara,
SACON, Coimbatore, India. Date of publication: 26 August
2023 (online & print)
Citation: Allen, M.L. & J.P. Kritzer (2023). Observations of Gray Fox Urocyon cinereoargenteus
(Schreber, 1775) (Mammalia: Carnivora: Canidae)
denning behavior in New Hampshire, USA. Journal of Threatened Taxa 15(8):
23662–23668. https://doi.org/10.11609/jott.8435.15.8.23662-23668
Copyright: © Allen & Kritzer 2023. Creative Commons Attribution 4.0
International License. JoTT allows unrestricted use, reproduction, and
distribution of this article in any medium by providing adequate credit to the
author(s) and the source of publication.
Funding: We are thankful for the funding provided by the Illinois Natural History Survey, Prairie Research Institute, and University of Illinois.
Competing interests: The authors declare no competing interests.
Author contributions: The authors contributed equally to the manuscript.
Acknowledgements: We thank the Illinois Natural
History Survey, and the University of Illinois for their support. R. Kritzer and B. Baldwin assisted with camera trap operations
and wildlife observations.
Abstract: Dens are important for mammals
because they provide protection for dependent young from weather and predators.
Gray Foxes Urocyon cinereoargenteus
are an understudied mesocarnivore that range across
North and Central America, and have limited
information available on demographics and denning behaviors. We monitored a
Gray Fox den in New Hampshire over the course of three years (2017–2020) to
quantify behaviors and document visitation and activity patterns of Gray Foxes
and other mammal species. We observed Gray Fox pairs intensively using the den
during parts of the first and second years of the study. Across the 949 trap
nights over which we monitored the den, use by adult Gray Foxes peaked in
spring – coinciding with the pup-rearing season. During this time, the adults
were diurnal with peaks in the afternoon, opposed to being crepuscular at other
times of the year. We did not observe any puppies during the first breeding
season, but during the second year we documented a puppy emerging from the den
on 24 May 2018. All excursions by the puppy outside the den for the first five
days were restricted to the immediate area near the den entrance and the puppy
was always with an adult when outside the den. During the puppy’s second solo
excursion, however, we documented a Bobcat Lynx rufus
pounce and kill the puppy, after which the adults abandoned the den. We also
observed the common (squirrels and rabbits) and uncommon (a bat) prey items
brought to the den, and the den being shared among multiple species. Our observations
highlight the importance of dens for protecting young, and our observations of
visitation and activity patterns, as well as common and uncommon prey, help
inform our understanding of the denning behavior of Gray Foxes.
Keywords: Activity patterns, den, mammal,
neonatal, predation, prey.
Introduction
Dens are important for mammals as
a means to protect the dependent young from weather and predators. Most canids
primarily use dens (generally holes dug in the ground) for raising young, and
while they may visit den sites throughout the year, activity often peaks from
mid-winter to early summer (Egoscue 1956; Chesemore 1969; Uraguchi &
Takahashi 1998). During this period, the pair bonds are often the strongest and
the mating pair act as central place foragers, which exhibits itself as the
pair often making foraging forays away from the den and returning with food
(Nicholson et al. 1985; Way et al. 2001; Allen & Moll 2023). Behaviors at
the den are often difficult to observe, and while there are many studies on
canid den selection, there are fewer studies documenting behaviors at dens (but
see Way et al. 2001; Elbroch & Allen 2013;
Mukherjee et al. 2018).
Gray Foxes Urocyon
cinereoargenteus are an understudied mesocarnivore that ranges across North and Central America
(Allen et al. 2022), and has limited information
available on demographics and denning behaviors (Allen et al. 2021). The
breeding cycle is generally thought to be from January through April, with
later dates in more northern areas (Sheldon 1949). The exact gestation period
is unknown and is often estimated as the same 53 days as Red Foxes Vulpes vulpes (Sheldon 1949). Litter size ranges from one to
six, with averages of three to four puppies (Sheldon 1949; Sullivan 1956; Wood
1958; Weston & Brisbin 2003; Glenn et al. 2009).
While Gray Foxes were traditionally thought to be monogamous, more recent
research shows that up to half of the litters exhibit multiple paternity (Glenn
et al. 2009).
Gray Fox dens can be in all
areas, including ground dens, cavities among rock piles or ledges, brush piles,
under buildings, and hollow logs (Sullivan 1959; Nicholson et al. 1985).
However, the use of dens appears to vary based on the stage of puppy rearing,
with only underground dens used during the weaning period, but hollow logs used
during whelping and nursing periods (Nicholson et al. 1985). Female movements
are similarly restricted by rearing stage, with movements greatly reduced
during whelping and nursing stages (Nicholson et al. 1985). Given that Gray
Foxes are often associated with forested habitats (Allen et al. 2021, 2002), it
is likely that den sites are often selected in forested areas similar to Red
foxes (Uraguchi & Takahashi 1998). However, Gray
Foxes prefer denning among denser cover and closer to water sources (Sullivan
1959).
We monitored a Gray Fox den in
New Hampshire over three years to quantify behaviors and document visitation
patterns of Gray Foxes and other species. We calculated the relative abundance
for all species using the den and the relative abundance, temporal patterns,
and duration of visits for Gray Fox adults and puppies. We also documented
predation of a puppy and prey items brought to the den by adult Gray Foxes.
Materials
and Methods
Study Area
We monitored a Gray Fox den in a
mixed forest area on private land in Strafford County, New Hampshire (43.114,
-70.918). Common tree species surrounding the den site include Eastern White
Pine Pinus strobus, Northern Red Oak Quercus
rubra, Red Maple Acer rubrum, American Elm
Ulmus americana,
and Black Birch Betula lenta. The surrounding
area is a low-density suburb consisting of generally wooded lots, with a number
of adjacent undeveloped conservation properties owned by municipal, state, and
non-profit landowners. Temperatures in the area reach wintertime lows below 00C
and summertime highs above 250C. Rainfall is moderate and relatively
consistent throughout the year, with monthly lows of approximately 70 mm in the
winter and around 100 mm in the spring and fall, but overall precipitation is
highest in the winter due to monthly snowfall that can exceed 300 mm. Mammal
species in the area are typical of the northeastern USA, including Black Bears Ursus americanus,
Bobcats Lynx rufus, Coyotes Canis latrans,
Fishers Pekania pennanti,
Raccoons Procyon lotor, Red Foxes, Striped
Skunks Mephitis mephitis, Virginia Opossums Didelphis
virginiana, White-tailed Deer Odocoileus
virginianus, and Woodchucks Marmota monax.
Field Methods
We first sighted a Gray Fox
traversing the property and entering the den in early February 2017, and again
in early April 2017. Following the second sighting, we set up a camera trap to
monitor the presence and activity of Gray Foxes and other species. We used a
Browning Recon Force (Model no. BTC-7FHD; Birmingham, AL, USA) to record a
burst of four images with two seconds between images when triggered, with a
1-minute delay between bursts. We ran the camera trap continuously from 13
April 2017, until 7 March 2020, with brief and infrequent gaps in coverage due
to dead batteries. The camera trap was mounted on a nearby tree 55 cm off the
ground and approximately 4.2 m from the den entrance. The field of view was
approximately 5 m wide by 2.5 m high, and centered on
the den entrance.
We observed Gray Fox pairs
intensively using the den during parts of the first and second years of the
study, but not during the third year (after which we ended the study). The den
was situated on a well-drained slope alongside a poorly drained and seasonally
flooded gully adjacent to several residential properties. Near-surface and
emergent granitic bedrock creates a variety of ledges, crevices, and other
structures along the slope. We could only confirm one entrance to the den,
although its interior structure is unknown and it is
possible other entrances might exist along the rocky ledge.
Statistical Analyses
We used program R version 4.2.2
(R Core Team 2022) for all statistical analyses. We calculated relative
abundance (RAB) on a monthly scale as:
RAB = visits / trap nights
to quantify the average number of
visits per day for each species, as well as gray fox adults and puppies. We
calculated the duration of visits to the nearest minute and calculated a
monthly average.
We used kernel density estimation
to quantify temporal activity patterns (Ridout & Linkie 2009). Our two comparisons were the overlap between
adults and puppies during the period when the puppy was active outside of the
den (24 May 2018 to 30 May 2018), and the overlap between adults during times
when they were intensively using of the den (April and May during 2017 and
2018) versus their use during the rest of the year. We used the time each visit
started as our values, after changing the time of each visit to radians that
corresponded to sun time. We then used the ‘overlap’ package (Meredith & Ridout 2017) to fit the data to a circular kernel density.
We estimated the activity among time periods from the kernel density
distribution. For our first comparison, we used due to small sample sizes, and in the second
comparison, used .
Results
Across the 949 trap nights we
monitored the den, we documented 27,072 photos, representing 3,205 independent
visits by animals. During the first year, the presumptive female (based on
smaller size) was distinctive by having a thin, uneven, and light-colored coat
with minimal characteristic markings. We observed the pair immediately and
consistently following installation of the camera trap on 13 April 2017,
through 26 May 2017 (Figure 1a). Thereafter, the Gray Foxes were observed only
occasionally near the den entrance and presumably had vacated the den. We did
not observe any puppies during the first breeding season.
After the den was vacated in May
2017, a pair of Gray Foxes began visiting and using the den periodically from
October 2017 through March 2018, before taking up regular residence again in April
2018 (Figure 1a). Both animals had more typical coats and markings, suggesting
that either the presumptive female from the first year had matured or regained
health, or that one or both individuals were different from those that had used
the den the previous spring.
During the second year of
observation, we first documented a puppy emerging from the den on 24 May
2018. For the first five days, the movement of the puppy was restricted to the
immediate area near the den entrance and the puppy was always with an adult
when outside the den. We never documented more than one puppy, and we assume
all observations were of the same individual. Overall, this encompassed a total
of 27 visits with an average duration of 21.9 minutes per visit. The puppy was
most active in the afternoons (Figure 2a), and during this time the activity of
adults was nearly a perfect mirror for activity of the puppy ( = 0.95).
On 29 May at 0451 h,
the puppy made its first solo excursion outside of the den, spending less than
one minute outside alone. On 30 May, the puppy emerged for its second solo
excursion at 0215 h and explored around the den entrance until 0225 h, when we
documented a Bobcat pounce and kill the puppy (Image 1). This was the first
visit we documented by a Bobcat since 9 May 2017. But the Bobcat
returned again twice on 30 May 2018 at 0253 h and 0322 h, both times
appearing to search around the den, with follow up visit on 01 and
02 June 2018.
Overall, use of the den by adult
Gray Foxes peaked in spring, coinciding with the breeding and pup-rearing
season (Figure 1a). Use of the den became more frequent each year in November, but was substantially more frequent in April and
May (Figure 1a). However, after Bobcat predation of the puppy in May 2018,
there was little activity at the den, with a few visits in January, February,
and March 2019 but no visits in any other months. During the two months that
adult foxes were actively using the den (April and May), they were most active
during the daytime, with peaks in the afternoon (Figure 2b). At other times of
the year, the activity of adult Gray Foxes was strongly crepuscular.
We documented adults returning to
the den with 51 prey items. Most of the prey items (n = 35) were not
identifiable in the photographs. The most common prey we could identify was
Eastern Gray Squirrels Sciurus carolinensis (n = 12) followed by Eastern Cottontails Sylvilagus floridanus (n = 3). The other notable
prey item that we observed was a bat of indeterminate species (Image 2).
Besides Gray Foxes (n = 1,029
visits), we documented visits by multiple species that also used the den,
including Striped Skunks (n = 316), Virginia Opossums (n = 207), and Woodchucks
(n = 140). Skunks and opossums used the den more frequently in the winter,
presumably for protection from the weather, whereas Woodchucks more frequently
used the den in summer and fall prior to hibernation (Figure 1b). Notably, we
observed Gray Foxes, skunks, opossums, and Woodchucks using the den close in
time to one another, reflecting den-sharing among these species. We also
documented other carnivores near the den site including Domestic Dog Canis
lupus familiaris (n = 51), Northern Racoon (n =
44), Domestic Cats Felis catus (n = 20), Bobcats (n = 14), Coyotes (n = 5), Red
Foxes (n = 5), Long-tailed Weasels Neogale frenata (n = 2), and a Fisher (n = 1). We also
documented other mammals, the most frequent of which included Eastern Gray
Squirrels (n = 731), Eastern Chipmunks Tamias
striatus (n = 454), and White-tailed Deer (n =
79).
Discussion
We documented Gray Foxes acting
as central place foragers and using the den as their focal area of activity.
The use of the den by Gray Foxes in the first and second year of monitoring
peaked in April and May, which coincides with the birthing season. We first
documented a puppy emerging from the den on 24 May in the second
year, and this was approximately the same time the den was vacated during the
previous year although we did not observe any puppies during the first year.
This could have been due to the female being immature or ill (e.g., mange), the
pair moving to a new birthing den, or the puppies dying in the den before
emergence. After the puppy was killed by the Bobcat in the second year, the
adults vacated the den and did not use it again the following year.
Our observations highlight the
importance of using dens for protecting young. Initially the Gray Fox puppy was
using the area outside of the den in the company of a parent, with the activity
patterns of the parents mirroring that of the puppy. This protection is helpful
because parents can signal danger to young (in which case young can retreat
into the den) and also potentially fight off other predators. When puppies are
outside of the den in the absence of parents, they are likely more prone to
predation and the second time we observed the puppy by itself outside of the
den it was killed by a Bobcat. The typical survival rates of juvenile Gray
Foxes (0.34) are often half that of adults (0.77) (Farias et al. 2005), with
predation being a common source of mortality for Gray Foxes. Predation is most
often attributed to Coyotes (Weston & Brisbin
2003; Farias et al. 2005), although Bobcat predation has also been documented
(Farias et al. 2005), along with legal harvest, vehicle collisions, and disease
(see review in Allen et al. 2021). While Gray Foxes are well known for their
ability to climb trees to escape predation, puppies are unlikely to be coordinated
enough to climb trees, emphasizing the importance of the den for safety.
Adult Gray Foxes are thought to
leave dens for short (~ one hour) hunting forays at crepuscular times to hunt
for food (Nicholson 1985). Although we found that Gray Foxes were crepuscular
at most times of year, they tended to be diurnal during times they were
intensively using the den (Figure 2b). We did not distinguish between behaviors
like sunning themselves outside of the den and hunting forays, and these
behaviors may occur at different times of day. We did document adults
frequently returning to the den with prey items, with larger prey (such as
squirrels and cottontails) and distinctive prey (bats) easier to identify. The
bat is notable because the scavenging of bats can lead to the transmission of
rabies (Theimer et al. 2017) and bringing a bat back
to the den increases risk for the entire family. It also raises the question of
how the Gray Fox acquired the bat. Eight species of bats reside in New
Hampshire, several of which roost primarily or opportunistically in trees where
Gray Foxes may hunt, but Gray Foxes are also known to scavenge bats (Theimer et al. 2017). Young animals need large quantities
of food, so parents likely bring whatever food is available back to the den.
While Gray Foxes often focus on common prey (e.g., squirrels, small rodents,
and rabbits), they have been documented bringing prey back to the den ranging
from Banana Slugs Ariolimax columbianus to deer (Elbroch
& Allen 2013).
In addition to our detailed
observations of Gray Fox behavior, we also documented interspecific den-sharing
among different combinations of Gray Foxes, Striped Skunks, Virginia Opossums,
and Woodchucks. Den-sharing entails trade-offs between costs such as
competition for space and increased pathogen exposure, and benefits such as
information sharing and
thermoregulation (Zeus et al. 2017). The balance of these trade-offs will vary
among the species in question and might not be reciprocal. For example, Cape
Ground Squirrels Xerus inauris,
Suricates Suricata
suricatta, and Yellow Mongooses Cynictis pencillatus
commonly share burrows in Namibia (Waterman & Roth 2007). Ground Squirrels
benefit from warning vocalizations by Suricates, but are at risk of predation on their juveniles by Yellow
Mongooses. Both Suricates and Yellow Mongooses
benefit from aggressive predator mobbing behavior by Ground Squirrels. Bats can
preferentially select roosts occupied by conspecifics or heterospecifics
due to the information conveyed about habitat quality (Zeus et al. 2017).
However, den-sharing among different species of Spiny Lobsters Panulirus spp. and Moray Eels Gymnothorax
spp. in shallow, tropical marine systems might be driven by habitat
limitation rather than any clear costs or benefits of cohabitation
(Lozano-Álvarez et al. 2007; Lozano-Álvarez et al. 2010). The extent to which
den-sharing among the species observed in this study represents costs-benefit
trade-offs or habitat limitation (i.e., lack of ideal dens) is unclear but may
affect the activity and conservation of these species.
For
figures & images – click here for full PDF
References
Allen, M.L.,
A.C. Avrin, M.J. Farmer, L.S. Whipple, E.P.
Alexander, A.M. Cervantes & J.M. Bauder (2021). Limitations of current knowledge
about the ecology of Gray Foxes hamper conservation efforts. The Journal of
Threatened Taxa 13: 19079–19092. https://doi.org/10.11609/jott.7102.13.8.19079-19092
Allen, M.L.,
A.M. Green & R.J. Moll (2022). Modelling the distribution and
intraguild associations of an understudied mesocarnivore
across the contiguous U.S.A. Diversity and Distributions 28(5):
1022–1033. https://doi.org/10.1111/ddi.13502
Allen, M.L.,
& R.J. Moll (in press). Prey dynamics before, during, and after red foxes
den on an urban university campus. Urban Naturalist.
Chesemore, D.L. (1969). Den ecology of the Arctic Fox in
northern Alaska. Canadian Journal of Zoology 47(1): 121–129. https://doi.org/10.1139/z69-021
Egoscue, H.J. (1956). Preliminary studies of the Kit
Fox in Utah. Journal of Mammalogy 37(3): 351–357. https://doi.org/10.2307/1376734
Elbroch, L.M. & M.L. Allen (2013). Prey indices and behaviors at a
Gray Fox den in San Mateo County, California. Western North American
Naturalist 73(2): 240–243. https://doi.org/10.3398/064.073.0215
Farias, V.,
T.K. Fuller, R.K. Wayne & R.M. Sauvajot (2005). Survival and cause-specific
mortality of Gray Foxes (Urocyon cinereoargenteus) in southern California. Journal of
Zoology 266: 249–254.
Glenn,
J.L.W., D.J. Civitello & S.L. Lance (2009). Multiple paternity and kinship
in the gray fox (Urocyon cinereoargenteus). Mammalian Biology 74:
394–402. https://doi.org/10.1016/j.mambio.2008.10.003
Lozano-Álvarez,
E., P. Briones-Fourzán, A. Osorio-Arciniegas,
F. Negrete-Soto & C. Barradas-Ortiz (2007). Coexistence of congeneric spiny
lobsters on coral reefs: differential used of shelter resources and
vulnerability to predators. Coral Reefs 26: 361–373.
Lozano-Álvarez,
E., P. Briones-Fourzán, L. Álvarez-Filip, H.M. Weiss,
F. Negrete-Soto & C. Barradas-Ortiz (2010). Influence of shelter
availability on interactions between Caribbean spiny lobsters and moray eels:
implications for artificial lobster enhancement. Marine Ecology Progress
Series 400: 175–185.
Meredith, M.
& M. Ridout (2017). Overview of the overlap package.
R project.
http://cran.radicaldevelop.com/web/packages/overlap/vignettes/overlap.pdf.
Mukherjee, A.,
H.N. Kumara & S. Bhupathy (2018). Golden Jackal’s underground
shelters: natal site selection, seasonal burrowing activity and pup rearing by
a cathemeral canid. Mammal Research 63: 325–339. https://doi.org/10.1007/s13364-018-0356-2
Nicholson,
W.S., E.P. Hill & D. Briggs (1985). Denning, pup-rearing, and
dispersal in the Gray Fox in east-central Alabama. The Journal of
Wildlife Management 49(1): 33–37. https://doi.org/10.2307/3801836
R Core Team
(2022). R: a
language and environment for statistical computing. R Foundation for
Statistical Computing, Vienna.
Ridout, M.S. & M. Linkie (2009). Estimating overlap of daily activity patterns from
camera trap data. Journal of Agricultural, Biological, and Environmental
Statistics 14: 322–337. https://doi.org/10.1198/jabes.2009.08038
Sheldon, W.G.
(1949). Reproductive
behavior of foxes in New York State. Journal of Mammalogy 30(3):
236–246. https://doi.org/10.2307/1375313
Sheldon, W.G.
(1953). Returns on
banded red and gray foxes in New York State. Journal of Mammalogy 34:
125.
Sullivan,
E.G. (1956). Gray Fox
reproduction, denning, range, and weights in Alabama. Journal of
Mammalogy 37(3): 346–351. https://doi.org/10.2307/1376733
Theimer, T.C., A.C. Dyer, B.W. Keeley,
A.T. Gilbert & D.L. Bergman (2017). Ecological potential for rabies
virus transmission via scavenging of dead bats by mesocarnivores.
Journal of Wildlife Diseases 53(2):
382–385. https://doi.org/10.7589/2016-09-203
Uraguchi, K. & K. Takahashi (1998). Den site selection and
utilization by the Red Fox in Hokkaido, Japan. Mammal Study 23(1):
31–40. https://doi.org/10.3106/mammalstudy.23.31
Waterman,
J.M. & J.D. Roth (2007). Interspecific association of Cape ground squirrels with two mongoose
species: benefit or cost? Behavioral Ecology and Sociobiology 61:
1675–1683. https://doi.org/10.1007/s00265-007-0398-y
Way, J.G.,
P.J. Auger, I.M. Ortega & E.G. Strauss (2001). Eastern coyote denning behavior
in an anthropogenic environment. Northeast Wildlife 56: 18–30.
Weston, J.L.
& I.L. Brisbin (2003). Demographics of a protected
population of Gray Foxes (Urocyon cinereoargenteus) in South Carolina. Journal of
Mammalogy 84(3): 996–1005. https://doi.org/10.1644/BOS-037
Wood, J.E.
(1958). Age structure
and productivity of a gray fox population. Journal of Mammalogy 39(1):
74–86. https://doi.org/10.2307/1376612
Zeus, V.M., S.J. Puechmaille & G. Kerth
(2017). Conspecific
and heterospecific social groups affect each other’s
resource use: a study on roost sharing among bat colonies. Animal Behaviour 123: 329–338. https://doi.org/10.1016/j.anbehav.2016.11.015