The Distribution of Amur Honeysuckle and Box Turtle Habitat Use in an Urban Forest
Omar Attum1,*, James Lowry1, Bruce Kingsbury2, and Evin Carter2
1Department of Biology, Indiana University Southeast, 4201 Grant Line Road, New Albany, IN 47150, USA. 2Department of Biology, Indiana University-Purdue University Fort Wayne, Fort Wayne, IN 46805, USA. *Corresponding author
Urban Naturalist, No. 12 (2016)
Abstract
Urban forests face major challenges to their ecological integrity because they are often small in size, surrounded by harsh edge-habitat, and can be vulnerable to colonization by invasive species. Lonicera maackii (Amur Honeysuckle) is considered one of the most problematic invasive species in the eastern US. In this study, we examined the distribution patterns of Amur Honeysuckle in an urban forest in Louisville, KY, USA, and the correlation between Amur Honeysuckle density and habitat use of Terrapene carolina (Box Turtle). We found no significant correlation between the density of young (<1 m tall) Amur Honeysuckle and distance to forest edge or hiking trails or density of mature (>1 m tall) Amur Honeysuckle and distance to forest edge. However, mature Amur Honeysuckle density increased as the distance from hiking trails increased. We also found no correlation between the density of young Amur Honeysuckle and Box Turtle habitat use, but at the landscape level, the likelihood of finding Box Turtles in an area decreases as the density of mature Amur Honeysuckle increases. Box Turtles were also more likely to be found in the vicinity of hiking trails than randomly selected points. Our results suggest that there is a negative correlation between mature Amur Honeysuckle density and Box Turtle habitat use, and that high densities of mature Amur Honeysuckle reduce available Box Turtle habitat.
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O. Attum, J. Lowry, B. Kingsbury, and E. Carter
22001166 URBAN NATURALIST No. 1N2o:1. –192
The Distribution of Amur Honeysuckle and Box Turtle
Habitat Use in an Urban Forest
Omar Attum1,*, James Lowry1, Bruce Kingsbury2, and Evin Carter2
Abstract - Urban forests face major challenges to their ecological integrity because they
are often small in size, surrounded by harsh edge-habitat, and can be vulnerable to colonization
by invasive species. Lonicera maackii (Amur Honeysuckle) is considered one of
the most problematic invasive species in the eastern US. In this study, we examined the
distribution patterns of Amur Honeysuckle in an urban forest in Louisville, KY, USA, and
the correlation between Amur Honeysuckle density and habitat use of Terrapene carolina
(Box Turtle). We found no significant correlation between the density of young (less than 1 m tall)
Amur Honeysuckle and distance to forest edge or hiking trails or density of mature (>1 m
tall) Amur Honeysuckle and distance to forest edge. However, mature Amur Honeysuckle
density increased as the distance from hiking trails increased. We also found no correlation
between the density of young Amur Honeysuckle and Box Turtle habitat use, but at the
landscape level, the likelihood of finding Box Turtles in an area decreases as the density of
mature Amur Honeysuckle increases. Box Turtles were also more likely to be found in the
vicinity of hiking trails than randomly selected points. Our results suggest that there is a
negative correlation between mature Amur Honeysuckle density and Box Turtle habitat use,
and that high densities of mature Amur Honeysuckle reduce available Box Turtle habitat.
Introduction
Urban forests face many challenges to their ecological integrity. They are often
small in size and are characterized by increased edge habitat that can be harsh and
vulnerable to colonization by nonnative invasive species (Ferreira and Laurance
1997, Hutchison and Vankat 1997, Murcia 1995, Pellissier et al. 2013). Furthermore,
sources of nonnative species including residential areas and other heavily
modified anthropogenic landscapes often surround urban forests.
Lonicera maackii (Rupr.) Maxim. (Amur Honeysuckle) is considered one of the
most problematic nonnative invasive species in forests of the eastern US (Luken
and Thieret 1996, Trisel and Gorchov 1994). Amur Honeysuckle was found to be
the most important plant species in terms of explaining variation in the composition
of woody plant communities within urban forests in Louisville, KY (Trammel
and Carreiro 2011). Amur Honeysuckle often outcompetes native shrubs, and its
establishment can lead to rapid modifications of ecosystems because it often attains
heights up to 6 m, creates high-density understory thickets, and has an extended
fruiting and leaf phenology that may modify environmental cues for native wildlife
(Carter et al. 2015, Mack et al. 2000, Smith 2013).
1Department of Biology, Indiana University Southeast, 4201 Grant Line Road, New Albany,
IN 47150, USA. 2Department of Biology, Indiana University-Purdue University Fort
Wayne, Fort Wayne, IN 46805, USA. *Corresponding author - oattum@ius.edu.
Manuscript Editor: Sonja Knapp
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2016 No. 12
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We would expect ectotherms to be negatively impacted by Amur Honeysuckle
because of the propensity of the species to invade early-successional habitat and
forest gaps. Forest edges and canopy gaps provide important thermoregulatory opportunities
and a diversity of food resources for ectotherms (Blouin-Demers and
Weatherhead 2002, Carter et al. 2015). Ectotherms often utilize canopy gaps to raise
or maintain internal body temperature in temperate forests (Row and Blouin-Demers
2006). The association between thermoregulation opportunities and habitat use and
the resulting effect on body temperature is recognized as a fundamental mechanism
that determines immediate physiological performance as well as long-term reproductive
success (Angilletta 2001; Bennett 1980; Huey and Kingsolver 1989, 2008;
Huey and Stevenson 1979; Kingsolver and Huey 2008; Scheers and Damme 2002).
Therefore, one expects that increased shade in the understory following invasion by
invasive species could affect habitat use and result in direct fitness impacts for ectotherms
(Carter et al. 2015, Hacking et al. 2014, Stellatelli et al. 2013).
In this study, we examined the relationship between Amur Honeysuckle distribution
and density and Terrapene carolina carolina L. (Eastern Box Turtle, hereafter
Box Turtle) habitat use in an urban forest.
Methods
Study species
Box Turtles utilize a wide range of habitats including upland and lowland
hardwood and pine forests, meadows, and the fringes of wetlands (Dodd 2001,
Greenspan et al. 2015, Kapfer et al. 2013). The species is a good model to study
the effects of Amur Honeysuckle at our study site because Box Turtles inhabit mesic
forests with high tree-cover, but are dependent for thermoregulation upon the
patches of open understory and forest edges that are vulnerable to Amur Honeysuckle
invasion (Dodd 2001). In addition, Box Turtles are omnivores that feed on a
diversity of plant and insect species often associated with forest-canopy gaps (Dodd
2001, Rossel et al. 2006). They are long-lived and typically have a home-range
size of 1–10 ha (Dodd 2001, Greenspan et al. 2015, Kapfer al. 2013). Box turtles
have experienced population declines throughout much of their range as a result
of land-use changes such as habitat destruction and degradation, and are a species of
conservation concern (Dodd 2001).
Study site
We conducted our study in Blackacre State Nature Reserve (BSNR) in Louisville,
KY (38.19611°N, 85.53416°W). The study site (44 ha) consists of an ~70-year-old
secondary-growth, urban forest dominated by Quercus rubra L. (Red Oak), Q. velutina
Lam. (Black Oak), and Acer saccharum Marshall (Sugar Maple). Other species
include Carya ovata (Mill.) K. Koch (Shagbark Hickory), C. laciniosa (Michx. f.)
G. Don (Shellbark Hickory), Gymnocladus dioicus (L.) K. Koch (Kentucky Coffee
Tree), Asimina triloba (L.) Dunal (Pawpaw), and Juniperus virginiana L. (Eastern
Red Cedar). BSNR is surrounded by residential neighborhoods, a railroad, and an
industrial park. Amur Honeysuckle is well established and appears to be the most
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O. Attum, J. Lowry, B. Kingsbury, and E. Carter
2016 No. 12
prevalent and widespread invasive species at BSNR. Other nonnative invasive species
include Lonicera japonica Thunb. (Japanese Honeysuckle), Rosa multiflora
Thunb. (Multiflora Rose), Eleagnus angustifolia L. (Russian Olive), Alliaria petiolata
(M. Bieb.) Cavara & Grande (Garlic Mustard), Sorghum halepense (L.) Pers.
(Johnson Grass), and Euonymus fortunei (Turcz.) Hand.-Maz. (Winter Creeper).
Field survey
During June and August 2011, we assessed the distribution and density of young
(1 m tall) and mature (≥1 m tall) Amur Honeysuckle at 380 random points within
BSNR as part of an existing monitoring program. We used a hand-held GPS (3-m
accuracy) to navigate to each survey point and record the number of Amur Honeysuckle
plants in each height class within a 3-m radius of the point. We calculated
density as the number of individuals per 3-m-radius circle. We examined the relationship
between density and distance from edge habitat as determined with GIS
software. We defined 2 types of edge habitat: forest edge as the perimeter of any
continuous gap > 4 m wide within areas of forest, and hiking trail.
We used radiotelemetry to monitor the movement patterns of 12 Box Turtles—3
females (mean mass = 426.6 ± SE 13.4 g, carapace length = 13.3 ± 0.04 cm) and 9
males (mean mass = 388.1 ± 7.9 g, carapace length = 12.75 ± 0.03 cm). We captured
the Box Turtles between May and August 2010, and glued radio transmitters to the
lateral-posterior end of the carapace with epoxy. The weight of the transmitters, ~10
g, was less than the maximum recommended 4–6% of body weight (Cochran 1980).
We attached transmitters in the field, and released the Box Turtles at their capture
site after the epoxy dried; all turtles were tracked the following year, ~2 times per
week from May to November 2011.
Each time a radiotelemetered turtle was located, we recorded the UTM coordinates,
date, time, and a suite of microhabitat characteristics within a 3-m radius at
each turtle location, including the number of young and mature Amur Honeysuckle
plants, percent upper-canopy cover (determined with a spherical densiometer),
leaf-litter depth, distance to nearest tree (diameter ≥ 20 cm), distance to nearest
fallen log (diameter ≥ 20 cm), and distance to nearest native shrub. In order to examine
microhabitat use, we collected equivalent data 20 m away from each turtle
location at a randomly selected direction (1–360°). We estimated activity-range
size using a minimum convex polygon (MCP).
Statistical analysis
We employed linear regression to look for a correlation between young and
mature Amur Honeysuckle density and distance to each edge category. We tested
whether the microhabitat at Box Turtle locations and random points 20 m away
was different through a backward stepwise logistic regression. We used separate
logistic regressions to test if Box Turtles avoided areas with high densities of young
and mature Amur Honeysuckle at the microhabitat and landscape level. At the microhabitat
level—habitat immediately available to the individual—we compared
Amur Honeysuckle density at the Box Turtle locations to the Amur Honeysuckle
density at the random points 20 m away. At the landscape level—the availability of
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microhabitat for the population at the study site—we compared Amur Honeysuckle
density at the Box Turtle location to the previously generated 380 random points
within the study site. We used logistic regression to test whether Box Turtles were
more likely to occur near hiking trails than other areas by comparing the distances
of Box Turtle locations from hiking trails and an equivalent number of random
points within a minimum convex polygon of all turtle locations. All data were normalized
by square-root transformation (sqrt [y+1]) prior to analysis.
Results
There was no significant correlation between the density of young Amur Honeysuckle
and distance to the edge habitats either when combined (F2,376 = 2.343,
t = - 1.208, P = 0.097), or when analyzed separately: distance to forest edge (B =
- 0.001 ± SE 0.001, t = - 0.850, P = 0.396) and distance to hiking trail (B = 0.001 ±
SE 0.001, t = 1.794, P = 0.074). There was no apparent correlation between mature
Amur Honeysuckle density and distance to forest edge (B = - 0.001 ± SE 0.001, t =
- 0.563, P = 0.57), but mature Amur Honeysuckle density increased with increasing
distance from hiking trails (B = 0.003 ± SE 0.001, t = 2.885, P = 0.004). However,
this model explained only 2.5% (r2 = 0.025) of the variation.
Mean activity-range of Box Turtles was 1.09 ha ± SE 0.093. There was no
significant difference between the measured microhabitats at turtle locations and
random points (χ2 = 2.89, df = 1, P = 0.48). Box Turtles were found in areas with a
mean upper-canopy cover of 82% ± SE 5.87, leaf litter depth of 7.79 cm ± SE 0.25,
at a distance of 2.72 m ± SE 0.11 away from a tree, 5.21 m ± SE 0.23 away from a
fallen log, and 0.183 m ± SE 0.032 away from a native shrub.
We detected no significant difference between young Amur Honeysuckle density
at the turtle locations and the random points at the microhabitat (χ2 = 0.014, df = 1,
P = 0.91) or landscape level (χ2 = 0.487, df = 1, P = 0.49; Fig. 1) or between mature
Amur Honeysuckle density at the turtle location and at the random locations at
the microhabitat level (χ2 = 2.894, df = 1, P = 0.09; Fig. 1). At the landscape level,
however, Box Turtles generally avoided areas with a high density of mature Amur
Honeysuckle (χ2 = 7.67 df= 1, P = 0.006; Fig. 1). Box Turtles were less likely to occur
in a given area as density of mature Amur Honeysuckle increased (Wald = 7.59,
B = 1.042 ± SE 0.38, df = 1, P = 0.006). Distance to hiking trails was a significant
predictor of Box Turtle distribution (χ2 = 72.346, df = 1, P < 0.001); Box Turtles
were significantly more likely to be observed near hiking trails (Wald = 59.719, B =
- 0.016 ± SE 0.002, df = 1, P < 0.001; 24.6 m ± SE 1.5 m) than the random points
(46.7 m ± SE 2.6 m).
Discussion
Neither distance to forest edge nor to hiking trails was a strong predictor of
Amur Honeysuckle density. Although the density of mature Amur Honeysuckle
was partially explained by distance to hiking trails, it explained only 2.5% of the
variation. Our findings suggest that either there may be other important predictors
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of Amur Honeysuckle density than those we tested or that Amur Honeysuckle has
successfully colonized all habitats at our study site equally and therefore has a
widespread distribution (Fig. 1). Colonization of forests by exotic invasive plants
is influenced by a variety of factors such as patch size, wildlife vectors, forest age,
light availability, and disturbance history (Hoffmeister et al. 2000, Masters and
Sheley 2001, Pellissier et al. 2013, Vellend 2002, Wimberly and Spies 2001).
Our results suggest that high density of mature Amur Honeysuckle reduces Box
Turtle habitat availability at the landscape level because Box Turtles were less likely
to be found in those areas (Fig. 1). Although the species is widespread at our study
site, we found lower densities of mature Amur Honeysuckle at both the turtle locations
and the nearby random locations (microhabitat sites) compared to densities at
random points scattered throughout the study site landscape; thus, Box Turtles seem
to utilize areas with lower densities of mature Amur Honeysuckle (Fig. 1).
The negative correlation between mature Amur Honeysuckle density and
Box Turtle locations at the landscape level may be the result of decreased
Figure 1. A comparison of Amur Honeysuckle density at turtle and random locations. Density
of young Amur Honeysuckle (less than 1 m tall) is represented with a black bar. Density of
mature Amur Honeysuckle (≥1 m tall) is represented with a white bar. Microhabitat represents
Amur Honeysuckle density at the random points 20 m away from the turtle locations.
Landscape represents Amur Honeysuckle density at random points generated at the landscape
level. * indicates a significant difference between mature Amur Honeysuckle density
at the landscape level and mature Amur Honeysuckle density at turtle locations.
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thermoregulatory opportunities caused by increased shade and lower temperatures
in the understory (Watling et al. 2011) or reduced food availability (Heleno et al.
2009). Box Turtle habitat use in temperate forests is largely believed to be shaped
by thermoregulatory opportunities and food availability; there is often a limited
availability of gaps in temperate forests (Dodd 2001, Rossel et al. 2006). Reptiles
in temperate forests bask in natural canopy gaps to increase their internal body
temperature through thermoregulation (Jaggi and Baur 1999, Pringle 2003). Amur
Honeysuckle may reduce thermoregulatory opportunities by increasing understory
shade in natural canopy gaps because invaded patches are significantly cooler than
intact forest patches (Carter et al. 2015). Forest patches invaded by Amur Honeysuckle
are characterized by a reduction and homogenization of environmental temperatures,
and these habitat modifications reduce the quality of thermal habitats for
ectotherms (Carter et al. 2015, Hacking et al. 2014, Stellatelli et al. 2013, Watling et
al. 2011). Carter et al. (2015) proposed that reduced thermoregulatory opportunities
and a reduction of thermoregulatory habitat quality was a main reason for the avoidance
of exotic vegetation by a temperate forest snake that occurs in the same region
in which we conducted our research. Other factors such as water and nesting-habitat
availability may be important, but we did not examine these variables during the
course of this study (Dodd 2001).
High density of mature Amur Honeysuckle may also reduce potential food
availability by reducing plant and insect diversity. Native plant diversity has been
found to be low in areas with high Amur Honeysuckle density because this species
outcompetes native understory plants for space and nutrients, and decreases light
availability (Collier et al. 2002). In addition, insect diversity and abundance are
often higher in canopy gaps (Horn et al. 2005) and lower in areas with high Amur
Honeysuckle density (Burghardt et. al. 2010). In contrast, we found no negative
correlation between Box Turtle habitat use and young Amur Honeysuckle, likely
because the young shrubs provide little understory shade. Carter et al. (2015) suggested
that invasive species associated with non-structural habitat modifications,
such as young plants or low-density areas may have relatively minor thermoregulatory
consequences for ectotherms.
We believe that Box Turtles were more common in the vicinity of hiking trails
because hiking trails and their margins are managed artificial canopy gaps in an
environment with reduced availability of natural canopy gaps. Other temperate
forest species are believed to use artificial canopy gaps created for recreational
use (Horn et al. 2005). For example, Agkistrodon contortix L. (Copperhead
Snake) were believed to regularly use maintained, understory artificial canopy
gaps for thermoregulatory purposes in a forest with a high density of invasive species
(Carter et al. 2014).
Urban forest management for temperate reptiles such as the Eastern Box Turtle
should focus on eradication of Amur Honeysuckle to increase habitat availability.
When complete eradication of Amur Honeysuckle is not feasible, we suggest
continuous maintenance and removal of mature Amur Honeysuckle around artificial
canopy gaps, creation of new artificial canopy gaps and Amur Honeysuckle-free
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zones, or reducing the foliage density (Carter et al. 2015, Inman et al. 2007). Community
structure and processes should be maintained by planting native midstory
plants in areas where Amur Honeysuckle has been removed (Hartman 2004). In this
study, we did not investigate the specific reasons that Box Turtles avoided areas
with high densities of mature Amur Honeysuckle, but our results suggest that Amur
Honeysuckle reduces habitat availability for Box Turtles.
Acknowledgments
This work was funded through Indiana University Southeast. We thank Dasynda
Rosenbarger, Christian Cutshall, Cheryl Nushard, Mary Smith, Misty O’Brian, and the
Conservation Biology class for their assistance in the field. In addition, we are grateful to
Susan Reigler for her logistical support, and Blackacre State Nature Preserve, Kentucky
State Nature Preserves Commission, and the Kentucky Fish and Wildlife Department for
their permission to sample on their land and for logistical support. The suggestions and
criticisms from the 2 anonymous reviewers helped improve the manuscript.
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