Biodiversity and Conservation
https://doi.org/10.1007/s10531-020-01990-y(0123456789().,-volV)(0123456789().,-volV)

ORIGINAL PAPER

Using spatial characteristics of apex carnivore
communication and reproductive behaviors to predict
responses to future human development
Veronica Yovovich1,3 • Maximilian L. Allen2 • Luke T. Macaulay3 •Christopher C. Wilmers1
Received: 27 July 2019 / Revised: 23 April 2020 / Accepted: 12 May 2020
Ó Springer Nature B.V. 2020

Abstract
A growing body of evidence has documented how wildlife alter their behavior in response
to human encroachment. For carnivores, behaviors related to reproduction and communication are particularly sensitive to human disturbance and can provide an early warning
indicator of development’s negative impacts. Despite the important role carnivores play inan ecosystem, few tools have been developed to anticipate how future human development
impacts these behaviors. We developed a set of models to understand spatial relationships
between anthropogenic development and puma (Puma concolor) habitat selection for two
critical reproductive behaviors: nursery habitat for raising young, and sites for communication with mates. Using geospatial location data from the Santa Cruz Mountains in
California, USA, we found that female pumas use small nursery home ranges (9 km2± 1.72 SE) of predominantly natural habitat, potentially with low levels of humandevelopment (\ 1 housing unit per 40 acres), when supporting kittens \ 8 weeks old.
Areas immediately surrounding (B 600 m) puma communication sites were also almost
entirely composed of undeveloped habitat or low-density development. When modelingprojected human development compared to current land use, we found that increases inhuman development may eliminate 20% of current puma nursery habitat and nearly 50% of
current communication site habitat. Future development will also increase the patchiness ofsuitable habitat, intensifying the difficulty of locating and accessing suitable areas fornurseries and communication. Focusing on the habitat needed to support reproductive andcommunication behaviors may be an effective way to prioritize conservation planning forpumas and other apex carnivores.
Keywords Anthropogenic development  Breeding habitat  Communication  Habitat
loss  Habitat selection  Puma concolor

Communicated by Xiaoli Shen.
& Veronica Yovovich
vyovovich@gmail.com
Extended author information available on the last page of the article

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Biodiversity and Conservation

Introduction
Early conservation efforts focused on setting aside large areas of land in order to preserve
intact ecosystems, but conservation goals can no longer be accomplished by establishingprotected areas alone (Wade and Theobald 2010; Wiersma and Sleep 2016; Kshettry et al.
2020). Increasing anthropogenic development necessitates creating viable conservation
strategies that promote coexistence with wildlife across rapidly changing landscapes(Burdett et al. 2010; Visconti et al. 2016; Kshettry et al. 2020). Exurban development is thefastest growing land use type in the U.S, and currently occupies 25% of the lower 48 states(Theobald 2001; Theobald 2005). Within the next 25 years, exurban development is
projected to increase by over 75%, with the highest rates of growth near coastal areas (Aliget al. 2004). Even modest growth in exurban areas may have large consequences forwildlife, making conservation planning for exurban areas critical (Burdett et al. 2010;
Krausman et al. 2011; Wiersma and Sleep 2016). Our study seeks to evaluate how populations of a wide-ranging carnivore, Puma concolor, might respond to such exurban
development. Specifically, we assess how two key behavioral characteristics, neonatal
nursery sites and communication scrape sites, might be impacted by current and future
development.
While some carnivore species may tolerate development (e.g. urban canids; Gehrt et al.
2010; Mueller et al. 2018), some species are displaced by areas with heavy human presence(Burdett et al. 2010; Wang et al. 2015; Vickers et al. 2015). Specifically focusing on pumas(Puma concolor), though they are not a wilderness-obligate species, there are no known
urban puma populations (Gehrt et al. 2010). Further, suburban and even exurban development may present significant impediments to puma use (Burdett et al. 2010; Vickers
et al. 2015; Benson et al. 2016). Pumas may live in open spaces adjacent to highly
developed areas, however, they spend the majority of their time utilizing undeveloped partsof their home ranges. Previous research has shown that puma reproductive and communication behaviors are particularly sensitive to human activities (Beier et al. 1995; Burdett
et al. 2010; Riley et al. 2014; Wilmers et al. 2013; Maletzke et al. 2017). Because nurseryand communication site selection are essential for puma population persistence, theirconservation is dependent on understanding how anthropogenic activity and development
affects these behaviors.
When pumas are supporting neonate offspring, they transition from occupying large
home ranges to localizing in a small area, adopting a central place foraging strategy as they
make limited forays from their den or nursery site to secure food (Beier et al. 1995; Logan
and Sweanor 2001). The areas surrounding nursery sites, or nursery home ranges, provide
critical resources that directly affect survival of dependent young and population dynamics(Ross et al. 2010; Davies et al. 2016). Relative to other life stages, neonate mortality isoften high, and neonates have high energetic demands. This makes selection of highquality nursery habitat critical for reproduction and survival (Logan and Sweanor 2001;
Laundré 2005). Understanding the specific habitat requirements during this restricted
nursery home range period can help inform predictions of how development will impact
future carnivore populations.
Communication sites are areas used for conspecific communication via scent marking
and are important for selecting mates and defining territories (Allen et al. 2015). Males
create communication sites, or scrapes, by using their hind feet to dig two shallow grooves
with a mound of soil and duff at one end, and will sometimes urinate or defecate on the
scraped mound of material (Allen et al. 2014). Male pumas communicate their presence to123Biodiversity and Conservationcompetitors using scrapes (Allen et al. 2016), and advertise to females for breeding
opportunities (Allen et al. 2015). Scrapes are often placed at prominent landscape locations, such as trail junctions, saddles, or under large trees. Communication sites are mostfrequently visited by males; however, these sites serve an important role to females as well
(Allen et al. 2014, 2015). When a female is ready to breed, she will often linger at theselocations and caterwaul to increase her chances of encountering a receptive mate (Logan
and Sweanor 2001; Allen et al. 2015).
The Santa Cruz Mountains of California, USA, ranging from urban Silicon Valley tolarge areas of preserved open space, provided a backdrop for quantifying how varying
levels of development affect puma behavior. Previous analyses conducted by Wilmers
et al. (2013) suggested that anthropogenic development plays a key role in shaping habitat
suitability for reproductive behaviors (i.e. communication and nursery sites), however thatwork did not assess the quality and characteristics of the habitat surrounding these sites.
Here we extend that analysis by explicitly estimating habitat selection by females during
their central place foraging phase (hereafter referred to as a nursery home range) andmodeled current and future human development patterns. This allows us to more accurately
model interactions between key puma behaviors and habitat availability in the context ofhuman development. We hypothesized that pumas would avoid anthropogenic development, and anthropogenic development in our study would increase, thereby shrinking
suitable habitat patches and increasing suboptimal matrix between patches.

Materials and methods
Study area
We conducted our study in the Santa Cruz Mountains of California, USA (Fig. 1). Our
1600 km2 study area ranged from sea level to approximately 1155 m in elevation, with two
distinct climactic zones: a cooler coastal climate on the west side, and warmer temperatures inland to the east. The climate was Mediterranean with hot, dry summers, and cool,
wet winters; most of the annual precipitation occurs as rain between November and April.
The study area encompassed a spectrum of human development and protected lands,
creating a mosaic of land use where human density ranged from 0 to 40 housing units peracre (0 to 9884 housing units per km2; see Table 1 for housing density categories anddefinitions). There were also large areas of preserved habitat managed by state, county, andcity parks as well as private entities. In between were areas with human influence ranging
from rural to urban development, as well as trails, fire roads, residential roads, andhighways.

Field methods
We captured 45 free-ranging pumas from 2008 to 2014 with cage traps, leg hold snares, ortrailing hounds as described in Wilmers et al. (2013). Puma capture, handling, and sampling protocols were approved by the Animal Care and Use Committee at the University ofCalifornia, Santa Cruz (protocol #Wilmc1101), and the California Department of Fish andWildlife. Individuals were tranquilized using Telezol (Fort Dodge Laboratories, Fort
Dodge, IA, USA) and fitted with a GPS/VHF tracking collar (GPS PLUS, Vectronics

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Fig. 1 Over the next 50 years, development is expected to greatly increase in the Santa Cruz Mountains,
California, USA. The fastest growing projected land use change between 2015 (a) and 2065 (b) will behabitat shifting from lightly modified development to exurban development

Aerospace, Berlin, Germany). Collars were programmed to acquire a GPS location every 4h, and the GPS data were remotely downloaded monthly via UHF, or transmitted via
cellular phone towers every 1–3 days depending on collar program configuration and cell
phone coverage.
We used female GPS collar data to locate potential nursery sites by searching forclusters of spatially aggregated GPS locations that persisted for [ 1 week, and werecharacterized by repeated excursions by the female to and from the site. In one instance,
the GPS collar failed and we used the collar’s VHF signal to repeatedly triangulate theposition of her nursery over the course of several days. We visited potential nursery GPS

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Table 1 Recent (2015) and predicted (2065) land cover statistics of each development category, and thepercent change from 2015 to 2065, for Santa Cruz, California, USA
Development category

Housing units per 100 km2

Percent of study
area
2015

2065

Percent changeLightly modified ([ 40 acres/house) \ 0.062

77.38

32.61

- 44.76

Exurban (2–40 acres/house)

0.062–1.236

6.43

49.23

? 42.8Suburban (0.25–1 acres/house)

1.236–9.884

11.07

12.63

? 1.56

Urban (\ 0.25 acres/house)[ 9.884

5.12

5.52

? 0.4

clusters between 3 and 6 weeks of when the female first localized to confirm the site as anursery by finding kittens or associated kitten sign. We then recorded the nursery coordinates using a handheld GPS unit, and subsequently monitored the female’s movements inrelation to the nursery as well as kitten fates.
We defined communication sites as frequently used scent marking areas containing C 3
scrapes within 9 m2 of one another (Allen et al. 2014). We located potential communication sites using an algorithm (described in full in Wilmers et al. 2013). The algorithm
located sites within 300 m of previous locations in which males visited, with visits separated by [ 7 days to eliminate feeding sites. Then we field-checked locations for scrapes
and recorded site coordinates with handheld GPS units. We also located communicationsites opportunistically during our extensive field activities, but sites identified by thealgorithm comprised the vast majority of communication sites recorded.

Model variables
We used a digitized housing layer (described in Wilmers et al. 2013) to classify the current
landscape into housing density categories as defined by Environmental Protection Agency
Integrated Climate and Land-Use Scenarios (ICLUS) model (Bierwagen et al. 2009)(Table 1). We employed a spatially explicit regional growth model (SERGoM) developed
by ICLUS (Bierwagen et al. 2009) to project future development in our study area (e.g.
Burdett et al. 2010). SERGoM uses several categories of input to create projections, withspecial attention to exurban/low-density development (Bierwagen et al. 2009). For ouranalyses, we used the ‘‘base case’’ development projection as a conservative prediction ofhuman development in Santa Cruz Mountains 50 years into the future (to the year 2065).
This assumes a ‘‘business-as-usual’’ development pattern and the midline U.S. Census
Bureau projection for population growth. For a detailed description of model assumptions,parameters, and alternative development patterns see Bierwagen et al. (2009). The SERGoM model produces a 100 m resolution raster of housing development categories.
We quantified habitat data by extracting landscape attributes for each point or area.
Prior to conducting statistical analyses, we used a correlation matrix to identify independent variable collinearity (|r| \ 0.50). All variables met this criterion and were retained in
the model. As a continuous variable, slope (x) was normalized as follows (Zuur et al.
2007),¼ ðxi  xmean Þ=std
xnorm
i

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When modeling future selection, we could not adequately predict distance to the nearest
road with the SERGoM model because the model output does not explicitly map roadlocations. However, the distance to roads had a marginal influence on site suitability, andthe SERGoM does implicitly incorporate road density into their model output. This
allowed our model to account for the influence of roads by including their effects as acomponent of development.

Statistical methods
We processed all spatial data in Geographical Information Systems program ArcGIS(v.10.1; ESRI, 2012) and R (v.2.1.3.1; R Development Core Team, 2010), and used R for
our statistical analyses. We used two packages in R: the lme4 package (Bates et al. 2015)
with a binomial link for model fitting, and the adehabitatHS package (Calenge 2006) forthe compositional analysis. We also used the LoCoH (Getz et al. 2007) and SERGoM(Bierwagen et al. 2009) tools in ArcGIS.

Home ranges
We used 95% adaptive local convex hulls (LoCoH; Getz et al. 2007) to estimate an annual
home range for each puma. We restricted our analyses to mature resident pumas because
subadult pumas are seldom involved in reproductive behaviors. We excluded data forpumas monitored fewer than 12 continuous months. To avoid overestimating home range
size due to shifts in territories, we used the first year of GPS data for individuals with dataspanning longer than 1 year (n = 24).

Modeling suitability: potential nursery home ranges in 2015
We assessed selection and avoidance in nursery home range areas in a use-availability
framework (Manly et al. 2002). This analysis considered the relationship between habitat
selection within animals’ home ranges (3rd order selection, sensu Johnson 1980) andlandscape features. We compared habitat characteristics in areas surrounding nursery sites
to similar areas within individual home ranges using a compositional analysis (Aebischer
et al. 1993). By defining used areas as ‘‘nursery home ranges,’’ or areas females utilized asa central place forager while she was bound to the nursery with young, immobile kittens,
this analysis allowed us to incorporate kitten-rearing behavior in nursery site selection. To
determine the effect of surrounding habitat, we compared nursery home ranges to comparably sized random areas selected within female home ranges. We modeled this behavior
by creating a nursery 95% LoCoH home range (Getz et al. 2007) for each nursery site byusing the GPS points collected while the female had kittens \ 8 weeks old. We createdcomparable ‘‘available’’ nursery areas by placing a buffer around each random point. The
buffer size was determined by sampling with replacement from a vector representing thesize of all used nursery home ranges. We then compared the percent composition of eachtype of anthropogenic development (Table 1) in used nursery home ranges compared tosimilarly-sized available areas, drawing 5:1 available:used areas at random from withineach female’s home range (Manly et al. 2002).
Next, we used the results from the nursery home range compositional analysis to model
landscape-level habitat suitability. Selected nursery home range habitat provided a metricfor suitable conditions, which we used in a moving window analysis to identify preferred123

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nursery area habitat within the study area. Specifically, we measured the percent composition of each development category (lightly modified, exurban, suburban, or urban) in
nursery home ranges, and used the mean (± SE) amount of each type of development
present to model suitable habitat across the study area. Positive t-values indicated apreference for the habitat type, and negative t-values indicated avoidance. For avoided
development categories, we used the mean value, plus the standard error, as the maximum
threshold for nursery home range suitability in our predictive model. For selected categories, we set the average value, minus the standard error, as the minimum threshold formodeling nursery home range selection. We used these mean values, plus or minus thestandard error, to model habitat suitability across the study area, as well as project how
suability will be influenced by development.

Modeling suitability: potential communication sites in 2015
Similar to the nursery analysis, we assessed selection and avoidance in communicationsites in a use-availability framework (Manly et al. 2002). We performed two analyses that
addressed selection at two different spatial scales—the first at the site, and the second at thearea around each site. In each analysis, we defined ‘‘used’’ points or areas as locations inwhich we found communication sites, and drew ‘‘available’’ comparison locations at
random from within each puma’s home range (mapped using a 95% LoCoH) at a rate of
5:1 available:used (Manly et al. 2002).
For the first communication site selection analysis, we modeled site-level selection
using a Resource Selection Function (RSF). The model variables were the four levels ofdevelopment, as a categorical variable, and slope (the terrain steepness, calculated using a
3 9 3 cell moving window), as a continuous variable. These two habitat features werepreviously identified as the most important for predicting communication site selection(Wilmers et al. 2013).
For our second analysis, we compared development and slope in areas surrounding
communication sites to equally-sized areas within individual home ranges. We quantified
differences in used and available areas by placing a 600 m radius circle around each used
and available communication site (Wilmers et al. 2013) and compared the slope and humandevelopment within used versus available areas using a compositional analysis (Aebischer
et al. 1993). Originally modeled by Wilmers et al. (2013), the 600 m buffers represent the
distance at which pumas are sensitive to human development when selecting communication sites.

Modeling future suitability: potential nursery and communication habitatin 2065
We mapped projected future housing density for the Santa Cruz Mountains for the year
2065 using the SERGoM GIS tool (Bierwagen et al. 2009). Using the tolerance/attraction
thresholds generated from our compositional analysis (Table 2a), we created a moving
window analysis to create binary (suitable/unsuitable) rasters for potential nursery homeranges and potential communication sites. In order to measure the distribution of suitable patches, we made a simulated puma home range grid with cell sizes the average sizeof a puma home range, and eliminated grid cells in urban areas, as these areas are
unsuitable habitat for a puma.

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Table 2 Human development in puma nursery and communication areas in the Santa Cruz Mountains,
California, USA in 2015
Development
category

Percent compositiona. Nursery
areas

SE

Communication
areas

SE

b. Female homerangesLightly modified

94.0

4.0

Exurban

3.5

1.3

Suburban

2.5

Urban

0.1

SE

Study
area

97.6

0.4

1.8

0.3

85.5

1.4

75.9

7.7

1.0

1.9

0.6

8.5

0.2

5.5

0.87

12.3

0.0

0.1

0.01

1.3

0.02

3.3

Mean values for human development in nursery home ranges and within 600 m of communication sites (a),and mean values for female home ranges and the study area as a whole allow comparison between
development levels in nursery areas (b)Values are reported as percentages of each development category

We generated nursery LoCoHs, and used the mean size of successful nursery patches asa minimum area required to raise kittens to an age beyond the use of the first nursery site.
In our analyses, we used binomial or quasibinomial regression to determine how projecteddevelopment will affect the properties and distribution of suitable patches and sufficiently
large patches and we incorporated slope into our modeled suitability using the estimatedparameter coefficient. The ability of the model to discriminate between communicationsites and non-communication sites was ‘acceptable’ as determined by an area of 0.79 under
the receiver operator curve (Hosmer and Lemeshow 2004).

Results
We used GPS data from 15 female and 14 male pumas, which were monitored for a meanof 636 ± 102 SE and 428 ± 52 SE days respectively. We recorded 119,787 locations for amean of 4130 ± 303 SE locations per animal. We documented 23 nursery home ranges for
12 female pumas (6 females had more than one nursery; Fig. 2). We also documented 299
communication sites from 13 males.

Nursery home range selection
The mean nursery home range area was 9 km2 ± 1.72 SE (Fig. 2). Though some nursery
home range areas contained low levels of exurban, suburban, or urban development, eachof the documented nursery sites themselves (n = 23) was located in the lightly modified
human development habitat category (Table 2). When selecting nursery home ranges,
female pumas preferred predominantly lightly modified habitat over any other housing
density category (compositional analysis: meannursery home range = 94% ± 4 SE, meanfemale home range = 86% ± 1 SE, p \ 0.01). Urban development made up a very small portionof the areas utilized while supporting young kittens (compositional analysis: meannursery home range= 0.0016% ± 0.0012 SE, meanfemale home range = 1.3% ± 0.02, p \ 0.01,
Table 2b).

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Fig. 2 Nursery home ranges in the Santa Cruz Mountains, California, USA between 2008 and 2014. An
illustration of the difference between annual home ranges (translucent) and nursery home ranges (smaller
opaque; area female utilized while maintaining a nursery), including urban and suburban areas in maroon. In
cases where females had multiple nurseries, they are shown by different shades of the same color. For visualclarity, only a subset of the total 23 nurseries is shown

Communication site selection
Similar to nurseries, every communication site was located in lightly modified habitat(n = 299), and communication area composition was predominantly lightly modified
habitat (Table 2). The RSF model suggested that male pumas significantly selected
communication sites in undeveloped habitat (b = 1.51 ± 1.032 SE) and relatively flatareas(b = 0.03 ± 0.124SE),andtheyselectedagainsturban
habitat(b = - 10.06 ± 309.12 SE; Table 3a). Similar to site-level conditions, males selected
undeveloped habitat within communication areas as well (compositional analysis: meanused= 98% ±0.35SE, meanrandom = 88% ± 1.00 SE, t299 = - 8.07, p \ 0.01; Table 3b).

Future landscape for suitable nursery and communication sites
Over the next 50 years, models predict that high levels of lightly modified development
will be converted to exurban development (Fig. 1). This shift would significantly reduce
currently suitable habitat for communication sites and nursery home ranges (Fig. 3). In
2015, 75.9% of our study area was categorized as very lightly modified, the areas modeled
as most suitable for nurseries and communicating, but by 2065 that number drops to 32.6%(Table 1). Every modeled female home range had sufficient nursery patches in 2015, or123

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Table 3 Models for puma communication site selection in 2015 in the Santa Cruz Mountains, California,
USA
Habitat VariableaCommunication RSF
Coefficient

Slope

0.03

SE

0.12

b
p

Compositional analysis
Mean percent
Used

Available

p

t

0.9

Development
category
Lightly modified

1.51

1.03

\ 0.01

97.59

88.35

\ 0.01- 8.07

Exurban

1.19

1.19

\ 0.01

1.80

6.82\ 0.01- 8.160.98

1.02\ 0.010.62

4.64\ 0.01- 6.28- 10.06

309.12

0.7

0.01

0.15

0.5

- 1.77

SuburbanUrban(a) Resource selection function results comparing development at communication sites with available sites
within male territories. (b) Compositional analysis results comparing the mean percent composition of eachdevelopment category found within a 600 m radius of communication sites and areas of the same size
randomly selected from male territories

Fig. 3 Changes in puma nursery and communication habitat between 2015 and 2065 in the Santa Cruz
Mountains, California, USA. The projected changes in spatial extent of suitable nursery habitat (in darkbrown; panels a and b) and suitable communication habitat (in blue; panels c and d) habitat between 2015
and 2065. The matrix (tan) is a mix of habitat types, ranging from urban development to undeveloped
natural habitats (namely mixed evergreen forest, redwood forest, oak savanna, chaparral, mixed oak forest,
coastal prairie and coastal scrub, and sandhills). Future suitable habitat for each behavior is projected toshrink and become more fragmented

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patches of continuous open habitat with low levels of urban, suburban, and exurban
development, while only 77% had sufficient patches in 2065. Future suitable habitat patches are also projected to become farther apart (Fig. 3), with the average distance between
sufficiently large nursery patches in 2065 projected to be three times the distance of 2015
(mean patch distance2015: 787 m ± 117 SE, mean patch distance2065: 2,749 m ± 260 SE;
p \ 0.01). A similar pattern was true for potential communication sites (Fig. 3). In 2015,
30% of the study area was considered suitable for communication sites, but our projectionsfor 2065 reduced potential communication site area to 18%. Overall, remaining potential
habitat is projected to shrink and became patchier, making suitable sites smaller and farther
apart.

Discussion
We explored the relationship between anthropogenic development and puma nursery andcommunication habitat, and found habitat suitability for these behaviors were vulnerable tocontinued human development. Although suitable habitat may be utilized for only a shortduration, pumas may breed at any time of year. Habitat suitable for breeding behaviors is
likely to be disproportionately important for puma survival, making it important to consider these areas in conserve efforts (Boitani and Fuller 2000). Our future development
projections suggest that nearly half of the lightly modified habitat that is key for these
reproductive behaviors will be converted to exurban and suburban development by 2065.
This would reduce available nursery habitat by 20% and potential communication habitatby nearly 50%, while making remaining habitat patchier and resulting in potential fitness
costs for the population (Hinam and Clair 2008; Burdett et al. 2010; Gehrt et al. 2010). By
explicitly modeling the spatial components of communication and nursery sites, we wereable to predict how animals are likely to respond to increased development and fragmentation and help inform conservation efforts. Future studies on conservation planning
may find it informative to explore spatial requirements for wildlife during sensitive periods(e.g., during the period of several weeks after giving birth when young are highly vulnerable). Focusing on the habitat requirements during infrequent, but highly important,activities may provide a critical tool for conservation planning efforts.
This study addresses female puma habitat use during the period in which they behave as
central place foragers while raising immobile kittens, and highlights habitat with highconservation value with respect to puma reproduction. These areas require protective coverfor kittens, as well as sufficient resources (prey, water, etc.) for the mother while supporting her growing young. When choosing nursery home ranges, female pumas avoided
human development. Every documented nursery site was located in undeveloped habitat(\ 1 housing unit per 100 acres), and females tolerated only small amounts of low-level
human development in areas surrounding the nurseries. This strong preference for undeveloped habitat likely has fitness implications, as habitat near humans has elevated populations of synanthropic carnivores (Wang et al. 2015) that could injure or kill vulnerable
kittens. Humans themselves may pose real risks, but even the perception of risk could
become taxing to a mother (Suraci et al. 2019). For example, when a female is disturbed,
she will often abandon kills she needs to feed her young, elevating energetic costs during aperiod that is already energetically expensive, and move her kittens to a new nursery site
(Logan and Sweanor 2001).

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Similar to females, males also selected lightly modified habitat at the site- and arealevel in relatively flat areas when creating communication sites. Pumas appear to selectsites that maximize their opportunities for communication between conspecifics (sensu
Allen et al. 2014), while minimizing interaction with human disturbance. The cues left at
communication sites are both chemical and physical (Allen et al. 2014), and vulnerable tohuman disruption. Hikers, cyclists, domestic dogs, and other recreationalists may trample,
mark over, or otherwise disturb communication sites, making communication sites better
suited to areas with little human impact. In the Santa Cruz Mountains, an aversion toprecipitous slopes greatly narrows the habitat available for scraping, and selecting against
human development reduces it further. Inadequate access to scrape habitat could generate
fitness costs from lack of communication with conspecific competitors and potential mates.
Future habitat development will likely alter the landscape for reproductive and communication behaviors. The habitat loss and increasing habitat patchiness projected in 2065
could confer large energetic penalties to female pumas and potentially reduce fecundity.
Habitat patchiness may leave some females without any access to optimal nursery habitat,
which could create an ecological trap in which females try to raise young in adverse
conditions. Similar to other carnivore species, neonate kittens experience a higher mortality rate than any other age group (Logan and Sweanor 2001). Nursing females are also
unable to traverse long distances in search of prey because they need to make kills to feedthemselves, and then quickly return to their young. Attempting to raise offspring in heavily
modified habitat would likely increase neonate mortality and shorten the inter-birthinterval. Pregnancy, lactation, and rearing young are energetically expensive, and the more
often these behaviors need to occur, the higher the cost (Oftedal and Girrleman 1989).
In addition to needing resources close to nursery sites, moving in more heavily fragmented habitat imposes other potential costs to females with young. Roads present a
dangerous direct and indirect challenge to wildlife in general (Bennett 2017), and pumas
specifically (Ernest et al. 2003; Riley et al. 2014; Vickers et al. 2015; Benson et al. 2016).
Reduced patch suitability and increased distance between patches in the future will likely
result in pumas crossing roads more frequently, and losing some patches from uncrossable
roads. In addition, living in close proximity to people, as predicted in model projections of
the future, exposes puma populations to increased human-derived mortality sources (e.g.
conflict with livestock or companion animals (Orlando 2008), anticoagulant rodenticide
exposure (Moriarty et al. 2012).
For males, limited access to suitable scrape sites could cause a breakdown of territorialboundaries and effective communication, increasing male–male conflict (Chanchani et al.
2018). Resident male pumas patrol their territories to refresh communication sites every 2
to 3 weeks (Allen et al. 2016). Males use scrapes to establish dominance as well as defineboundaries (Allen et al. 2015), allowing competing males to avoid physically confronting
one another (Logan and Sweanor 2001). Intraspecific strife can be an important population
driver (Rankin 2007), especially as isolation from other puma populations increases (Riley
et al. 2014). The impacts could range from low cost outcomes, such as inefficient use oftime or energy, to fitness costs including bodily harm or death.
Communication sites also serve as a way for males to advertise themselves to potential
mates (Allen et al. 2014) and provide a location for females to communicate their
receptivity to breeding (Allen et al. 2015). Without these sites, males and females could
have a more difficult time finding mates, resulting in decreased reproductive success acrossthe population (e.g., Slabbekoorn and Ripmeester 2008). Breeding success is correlatedwith territory maintenance, as kittens are generally sired by a territory-holding male
(Logan and Sweanor 2001; Allen et al. 2015). Thus, the ability to secure and hold a123Biodiversity and Conservation

territory can have significant implications for reproductive success of a particular male,with broader population-level implications as well (Logan and Sweanor 2001).
Historically, pumas were widely distributed, occupying nearly every habitat in theAmericas from the desert to tropical rain forests (Logan and Sweanor 2001), suggesting ahigh degree of adaptability. Our analyses did not take into account behavioral plasticity to
an increasingly human-dominated landscape, and with diminished access to ideal sites,
pumas may compensate to some degree by substituting less preferred sites. Pumas havedemonstrated the ability to adapt and persist in urban- or suburban-adjacent areas (Burdett
et al. 2010; Riley et al. 2014). However, evidence suggests they are less adaptable topersisting within more developed environments than many other carnivore species, such as
coyotes or foxes (Gehrt et al. 2010); puma populations studied in areas adjacent to humandevelopment have suffered from inbreeding depression and population declines (Burdett
et al. 2010; Vickers et al. 2015; Benson et al. 2016; Gustafson et al. 2019). Our study area
is situated in an area already highly impacted by people; local puma population genetics
show a relatively high degree of inbreeding and isolation (Gustafson et al. 2019), which
could indicate that they are already living on the lower end of their acceptable spectrum. Ifthey are currently subsisting in suboptimal habitat, further flexibility may not be possible.
In addition, increased development will likely have additional negative implications fordispersal permeability and gene flow (Riley et al. 2014; Vickers et al. 2015; Gustafson
et al. 2019) and overall habitat loss (Burdett et al. 2010; Visconti et al. 2016).
Our study highlights the need for regional planning to pay special attention to development patterns. In the next 50 years, 96% of the land use change is predicted to transformcurrently suitable habitat to lower quality, non-preferred exurban development (Table 1;
Fig. 1). Redirecting some of this development into higher density, more efficient development in suburban or urban areas would allow space for humans and wildlife populations
to coexist. The pervasiveness of habitat loss and transformation make it all the more
important to carefully develop around remaining habitat (Burdett et al. 2010; Wang et al.
2015; Visconti et al. 20165; Maletzke et al. 2017). We modeled the relationship between
pumas and human development in the Santa Cruz Mountains, but these dynamics are likely
playing out across puma’s large distribution and our findings are likely transferrable toother carnivore species as well. In addition, gaining a better understanding of how habitat
modification influences wildlife can also help garner public support for sound conservation
practices, and guide future development plans to ensure that wild populations can thrivealongside human development.
Acknowledgements We thank the California Department of Fish and Wildlife for their support of funding
and staff; C. Wylie and D. Tichenor for their support capturing pumas; Y. Wang, P. Houghtaling, J. Smith,
Y. Shakeri, and dozens of interns for their time and efforts; (A) Cole and (B) Nickel for their tireless GIS
guidance; the many landowners who allowed us access to their property; and the National Science Foundation, Moore Foundation, American Museum of Natural History, and UC Santa Cruz Environmental
Studies Department for their generous funding.

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Afﬁliations
Veronica Yovovich1,3 • Maximilian L. Allen2 • Luke T. Macaulay3 •Christopher C. Wilmers1
1

Environmental Studies Department, Center for Integrated Spatial Research, University ofCalifornia, 1156 High St., Santa Cruz, CA 95064, USA

2

Illinois Natural History Survey, University of Illinois, 1816 S. Oak Street, Champaign, IL 61820,
USA

3

Environmental Science, Policy, and Management, University of California, 145 Mulford Hall,
Berkeley, CA 94720, USA

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