NOTES AND FIELD REPORTS
Chelonian Conservation and Biology, 2010, 9(1): 131–135
g 2010 Chelonian Research Foundation
Impacts of Anthropogenic Structures on
Predation of Painted Turtle
(Chrysemys picta) Nests
JERAMIE T. STRICKLAND1 AND FREDRIC J. JANZEN1
1
Department of Ecology, Evolution, and Organismal Biology,
Iowa State University, 253 Bessey Hall, Ames, Iowa 50011 USA
[Jeramie_Strickland@fws.gov; fjanzen@iastate.edu]
ABSTRACT. – Anthropogenic factors can negatively
impact wildlife populations, but deleterious effects
may not be universal. We investigated the relationship
between nest predation and spatial proximity to
anthropogenic structures (campsites, trash bins, etc.)
for 1375 painted turtle (Chrysemys picta) nests over
6 years for a population on the Mississippi River,
Illinois. Although varying among years, the probability of nest predation increased with greater distance
from anthropogenic structures over all years combined and did not differ between supplemental food
attractant structures (e.g., fish cleaning table) and
nonsupplemental food attractant structures (e.g.,
horseshoe pits).
Habitat alteration or other human activity can
influence wildlife populations in multiple ways, including
those that are spectacularly or subtly detrimental. For
example, roads that bisect habitats can serve as a direct
(e.g., animals struck by vehicles; Gibbs and Shriver 2002;
Steen and Gibbs 2004; Aresco 2005) or indirect (e.g.,
enhanced predation of nests along habitat edges; Temple
1987) source of mortality in turtles. These human impacts
also can vary substantially both temporally and spatially.
For example, lightly traveled roads should have a low
direct effect on wildlife mortality, but the impact should
increase when traffic is heavy.
Human activity can also influence predator–prey
interactions involving turtles, potentially in complex ways.
For example, supplementing predators with human-derived
food can enhance population size of predators and,
subsequently, alter prey numbers (Vander Lee et al.
1999; Hamilton et al. 2002). In avian systems, some
131
predators incidentally find nests while foraging for
alternate food (Vickery et al. 1993). Thus, anthropogenic
structures associated with supplemental food may attract
predators and increase predation on nearby nontarget turtle
nests. Despite the potential for anthropogenic factors to
impact wildlife populations, the indirect effects of humanderived supplemental food have been poorly studied.
Turtle nests and their predators are a good system for
examining spatiotemporal variation in the effects of
anthropogenic structures on turtle nest predation. Nest-site
choice is crucial for turtles (Refsnider and Janzen 2010), as
mortality rates are highest during embryonic development
(Ernst and Lovich 2009) and predation is responsible for
the majority of nest mortality (Congdon et al. 1983;
Schwanz et al. 2010). In addition, the location of a nest may
increase offspring vulnerability to predation prior to (Kolbe
and Janzen 2002a) and after (Kolbe and Janzen 2001)
emergence. Thus, nest success is a key determinant of
recruitment rates in many turtle populations, and high nest
mortality has caused some turtle populations to decline
(Gibbons 1968). Furthermore, inadvertently supplementing
predators with food via garbage, bird feeders, and so on
may reduce predation on turtle nests, yet other studies
suggest that such supplemental foods can increase
predation on nests (Cooper and Ginnett 2000). These
conflicting results warrant further investigation, especially
since turtles comprise a globally imperiled taxon (Buhlmann et al. 2009).
We evaluated 6 years of data to investigate the
temporal and spatial effects of anthropogenic structures
on predation of painted turtle (Chrysemys picta) nests at
the Thomson Causeway Recreation Area (TCRA) in the
Mississippi River near Thomson, Illinois (Kolbe and
Janzen 2002b; Schwanz et al. 2010). Using this 450 3
900-m human-impacted island, we tested 3 hypotheses: 1)
turtle nests located closer to anthropogenic structures
generally suffer higher predation, 2) spatial patterns of
predation on turtle nests change with annual intensity of
nest predation, and 3) probability of nest predation
increases with proximity only to anthropogenic structures
associated with supplemental food.
Methods. — The TCRA includes a recreational
vehicle campground that contains a circular road,
benches, campsites, trash bins, a fish-cleaning table,
horseshoe pits, and toilet facilities. At least some of these
anthropogenic structures at the TCRA may contain
attractants, such as supplemental food, for nest predators,
which are mainly raccoons (Procyon lotor) (Kolbe and
Janzen 2002b). Because anthropogenic structures are
situated within the nesting habitat of painted turtles, we
compared predation between nests that were laid closer
vs. farther from the anthropogenic structures identified
previously.
The predation status of each nest was monitored at
least every 3 days from oviposition until the end of the
nesting season (mid-May to late June). Depredated nests
were detected by observing broken eggshells outside the
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BIOLOGY, Volume 9, Number 1 – 2010
Table 1. Effects of distance from the closest anthropogenic structure on predation of painted turtle (Chrysemys picta) nests. Predation
levels and number of nests laid for each year of this study are followed by results from logistic regression analyses, with the distance
from closest anthropogenic structure as the independent variable and nest fate as the dependent variable.
Year
% Predated
Number of nests
Slope estimate
p-value
Standard error
1997
1998
2000
2001
2003
2005
19.7
198
20.0351
0.3830
0.04
35.9
178
20.1678
0.0010
0.04
59.1
168
20.1223
0.0023
0.04
89.5
215
0.0138
0.1243
0.09
57.1
326
0.0874
0.0006
0.03
95.8
285
0.0073
0.9209
0.07
nest, clear excavation of the nest cavity, and absence of
intact eggs in the nest. In mid-September of each year, all
remaining nests were excavated and any eggs or
hatchlings noted, and final predation status (depredated
or intact) was determined. Intact nests at the end of the
nesting season were determined in September to have
been depredated if a conspicuous, empty hole was
observed in the ground at the nest site.
The objective of this study was to determine whether
nest predation varied across the nesting habitat as a
function of distance from anthropogenic structures. In
addition, we evaluated which types of anthropogenic
structures influenced nest predation. If nest predation
varies as a function of proximity to or type of
anthropogenic structure, the data can be partitioned
appropriately to further address questions related to
spatial-dependent predation. Nest predation and nest
location data over 6 years (1997, 1998, 2001–2003,
2005; total number of turtle nests 5 1375) were used to
test the hypothesis that probability of nest predation is
greater near anthropogenic structures. Nest predation
intensity has fluctuated significantly, ranging from as low
as ca. 20% in 1997 to as high as ca. 96% in 2005. We
compared patterns of nest predation between low (ca.
30%), medium (ca. 60%), and high (ca. 90%) years.
Therefore, we chose to analyze data for years when
overall nest predation was similar to these low, medium,
and high rankings.
Logistic regression (SAS Institute 2008) was used to
test whether nest predation increased or decreased with
distance from an anthropogenic structure. The probability
that a nest was depredated was modeled where the
response variable was categorical (1 5 depredated,
0 5 intact) and the predictor variable (distance from
closest anthropogenic structure) was continuous. We
further tested the possible impact of supplemental food
attractant structures (e.g., fish table, camper pad, trash
bin) vs. nonsupplemental food attractant structures (e.g.,
road, benches, toilet facilities, horseshoe pits) on
probability of nest predation, with the latter category
serving as a control for any general impact of anthropogenic structure. Distance to the closest anthropogenic
structure for each nest was scaled to the nearest meter to
accommodate imprecision (e.g., a nest located 7.39 m
from a trash can would be scaled to 7 m). The scaled
measurements were then used to assess whether nests laid
closer to such structures were more likely to be
depredated. To evaluate the probability of nest predation
as a continuous function of distance to closest anthropogenic structure, we used a cubic spline technique
originally developed for visualizing natural selection
(Schluter 1988; see also Kolbe and Janzen 2002b).
Standard errors for the spline were calculated by
bootstrapping the data 50 times.
Measures derived from the Akaike information
criterion (AIC) were used to select the model that best
described the data. Our model selection procedure helped
us to identify which variables were important in
influencing nest predation. All interactions and combinations of variables (anthropogenic structures and distance
to closest anthropogenic structure) were run using logistic
regression, and then each model was assessed using AIC,
specifically QAIC (Burnham and Anderson 1998). The
lowest QAIC value indicated the best model among the
alternate models examining the data.
Results. — Nests in closer proximity to all anthropogenic structures were more likely to experience
predation in 2 of the 6 years (1998 and 2000) used in
the analysis in comparison to nests farther from
anthropogenic structures (Table 1). However, in 2003,
nests laid farther from anthropogenic structures were
more likely to experience predation. In other years (1997,
2001, 2005), all of which had especially high or low
predation intensity (Table 1), we did not detect a pattern
of nest predation in relation to distance from anthropogenic structures.
Over all 6 years, we found a significant, positive
relationship between the probability of nest predation and
nest distance from anthropogenic structures (Fig. 1;
Table 2). The model with the lowest AIC value did not
include type of structures separately or individually (e.g.,
benches, toilet facilities, camper pads, horseshoe pits, or
road). Instead, this model included only distance to
closest anthropogenic structure, regardless of type. In
general, our model predicted that probability of nest
predation should increase modestly but significantly with
distance from an anthropogenic structure (e.g., 0.69 at 10m distance vs. 0.59 at 1-m distance) (Fig. 1). This
NOTES AND FIELD REPORTS
133
Figure 1. Cubic spline analysis of the probability of predation on nests of the painted turtle (Chrysemys picta) with increasing
distance from anthropogenic structures. Results for all 6 years of this study combined are shown. Dashed lines bracketing the spline
(solid line) represent standard errors calculated by bootstrapping the original data 50 times.
outcome contradicted the hypothesis that nests closer to
anthropogenic structures should experience higher predation.
We explored this relationship in more detail by
testing whether there was a significant difference between
structure type and spatial probability of nest predation
(Table 3). We found no evidence that nest predation
depended on distance to any particular type of structure.
Nonetheless, nests located relatively close to an anthropogenic structure had a higher probability of avoiding
predators, further supporting the findings of the ‘‘reduced’’ model (Table 2).
We further tested the possible impact of supplemental
food attractant structures vs. nonsupplemental food
attractant structures on probability of nest predation
(Table 4). In a model accounting for the food vs. nonfood
nature of anthropogenic structures and nest distance from
structure, we found that the nature of the structure was not
significantly related to the probability of predation.
Instead, as before, nests located farther from humanmade structures had higher probabilities of predation
(Fig. 1). Thus, at this field site, anthropogenic structures
most likely to possess supplemental food did not affect
the odds of predation on proximal turtle nests.
Discussion. — Nest-site choice is critical for
successful breeding in a wide range of oviparous taxa
(Refsnider and Janzen 2010). Nest-site choice is important for turtles, not least because nest predation is
naturally high in most populations. Of increasing
relevance, anthropogenic activities could alter predator
behavior, influencing nest success and thereby affecting
the persistence and survival of declining turtle populations. In our study, we examined the effects of distance
from anthropogenic structures on nest predation in a
population of painted turtles. We showed that, in some
years, turtle nests are subject to predation pressure that is
inversely related to the proximity of nests to anthropogenic structures. In contrast, logistic regression and cubic
spline analyses over all years combined revealed that
probability of predation on turtle nests was positively
correlated with distance from any anthropogenic structure, indicating that nests located closer to anthropogenic
structures were less likely to encounter predation. Still,
the annual differences observed in the logistic regression
results suggest that more years of data are necessary to
develop a better understanding of these processes. Even
so, we found no significant evidence of a difference in
spatial-dependent predation between different types of
anthropogenic structures.
Field experiments to examine patterns of turtle nest
predation provide another perspective on our observational findings. Experimental studies strongly implicate
Table 2. Models of predation on painted turtle (Chrysemys picta) nests ranked by QAIC value. The best model indicates that only
distance to any anthropogenic structure influences probability of predation on nests, regardless of structure type or possible
relationship to supplemental food.
Explanatory variable (parameter)
Distance
Anthropogenic structure (type)
Supplemental food attractant structure vs. nonsupplemental food
attractant structure
x2
p-value
df
QAIC value
6.7466
4.2120
0.0094
0.3871
1
4
803
807
0.7135
0.7135
1
813
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BIOLOGY, Volume 9, Number 1 – 2010
Table 3. Model testing for an effect of distance and type of
anthropogenic structure on probability of predation on nests of
the painted turtle (Chrysemys picta). All parameters were
compared to the road, with only distance to all structures
yielding a significant result.
Table 4. Effects on predation on nests of painted turtles
(Chrysemys picta) of distance and supplemental food attractant
structures (e.g., camper pad, trash can, fish table) vs.
nonsupplemental food attractant structures (e.g., road, horseshoe
pits, toilet facilities, benches).
Explanatory variable
(parameter)
Parameter
df
Estimate
SE
x2
p-value
Intercept
Distance
Structure
1
1
1
1.1770
0.0457
20.0825
0.1184
0.0225
0.0977
98.8829
4.1326
0.7135
, 0.0001
0.0421
0.3983
Distance
Benches
Toilet facilities
Camper pads
Horseshoe pits
Trash can
Fish table
x
2
4.733
0.231
1.644
0.292
3.210
1.734
0.323
p-value
df
Slope
SE
0.0296
0.6305
0.1997
0.5888
0.0732
0.6105
0.6170
1
1
1
1
1
1
1
0.0492
20.1961
20.6627
20.1142
20.5092
20.1847
20.1098
0.0226
0.4076
0.5168
0.2113
0.2842
0.4264
0.3047
visual cues as a primary means by which raccoons locate
turtle nests (Strickland et al. 2010), although such nest
predators also possess excellent olfaction (Conover 2007).
These sensory capabilities might cause nonhabituated
raccoons to be deterred by anthropogenic structures,
assuming they have a fear of humans or pets (e.g., dogs),
even when supplemental food is associated with such
structures. Numerous campers who visit the TCRA own
dogs, which could cause turtle nests located farther from
anthropogenic structures to suffer a higher probability of
predation from raccoons.
Variation in predator–prey interactions as a function
of anthropogenic activities may alter nest survival
(Vander Lee et al. 1999; Bowen and Janzen 2008).
Anthropogenic structures reduced recruitment in some
(but not most) years in our study, yet generalizations
regarding the negative impacts of anthropogenic structures should be made with caution (sensu Hamilton et al.
2002). Moreover, although predation on painted turtle
nests at the TCRA is greater closer to ecological edges in
some years (Kolbe and Janzen 2002b) and exhibits
evidence of positive density dependence (Valenzuela
and Janzen 2001), we did not explicitly account for those
2 variables in our study. Still, the lack of enhanced
predation near anthropogenic ‘‘edges’’ where nest
numbers are often higher (e.g., camper pads) suggests
that habitat edges and nest density did not play important
roles in our study. Regardless, studies of the behavior of
nest predators at the TCRA would greatly enrich our
understanding of the predation patterns that we detected.
Our results did not reveal a significant difference
between the food attractant structures and the nonsupplemental food attractant structures in probability of
predation on proximal turtle nests. Therefore, supplemental food attractant structures may not influence the
foraging success of turtle nest predators at this particular
study site. Alternatively, supplementing predators with
food resources may be a way to reduce nest predation, at
least in birds (Crabtree and Wolfe 1988; Vander Lee et al.
1999). Furthermore, Boag et al. (1984) and Miller and
Hobbs (2000) suggested that predation risk on bird nests
tended to decrease with lesser distance from anthropogenic trails in their study. In contrast, Miller et al. (1998)
reported an increase in predation on bird nests located
near anthropogenic trails.
Our study has broad implications for conservation of
ground-nesting species because any anthropogenic activities that attract or deter additional predators could impact
such species. For example, campers and visitors should
avoid leaving trash or any other supplemental food items
in such habitats, especially during the turtle nesting
season, given that our results show that distance to
anthropogenic structures could directly or indirectly
influence nest predation rates. Indeed, human activities
could be critical because persistence of this turtle
population (and probably most) depends on substantial
survival of nestlings (Schwanz et al. 2010). Thus, results
from our research on a common, easily studied turtle may
inform conservationists about strategies for protecting
other species with similar nesting behaviors and life
histories.
Future emphasis should be geared towards modeling
nest survival times to see if nests that are laid closer to
anthropogenic structures are depredated more quickly
than nests that are laid farther away. This assessment can
be done using survival times (e.g., proportional hazard
analysis). Additional studies are necessary to quantify the
long-term effects of anthropogenic structures on the
population dynamics of turtles and their nest predators.
ACKNOWLEDGMENTS
We thank the U.S. Army Corps of Engineers, the U.S.
Fish and Wildlife Service, and the Illinois Department of
Natural Resources for allowing us to conduct this research
on their field site; the 1997–2008 Turtle Camp field
crews, T. Mitchell and K. Lundquist, for assisting with
data collection; the entire Janzen lab for reviewing
proposals and manuscripts; A. Trapp II, J. Church, L.
Kasuga, R. McNeeley, E. Otárola-Castillo, D. Warner,
and the Iowa State University Statistics Consulting group
for assisting with the statistical analyses; W. Clark and D.
Debinski for general guidance; and L. Luiselli and J.
Rowe for constructive criticisms on the manuscript. The
Graduate Minority Assistantship Program and the Agricultural Experiment Station at ISU supported JTS. An
Ecological Society of America SEEDS Special Project
grant and a National Science Foundation grant DEB0604932 to FJJ provided funding for this research.
NOTES AND FIELD REPORTS
LITERATURE CITED
ARESCO, M.J. 2005. The effect of sex-specific terrestrial
movements and roads on the sex ratio of freshwater turtles.
Biological Conservation 123:37–44.
BOAG, D.A., REEBS, S.G., AND SCHROEDER, M.A. 1984. Egg loss
among spruce grouse inhabiting lodgepole pine forests.
Canadian Journal of Zoology 62:1034–1037.
BOWEN, K.D. AND JANZEN, F.J. 2008. Human recreation and the
nesting ecology of a freshwater turtle (Chrysemys picta).
Chelonian Conservation and Biology 7:95–100.
BUHLMANN, K.A., AKRE, T.S.B., IVERSON, J.B., KARAPATAKIS, D.,
MITTERMEIER, R.A., GEORGES, A., RHODIN, A.G.J., VAN DIJK,
P.P., AND GIBBONS, J.W. 2009. A global analysis of tortoise
and freshwater turtle distributions with identification of
priority conservation areas. Chelonian Conservation and
Biology 8:116–149.
BURNHAM, K.P. AND ANDERSON, D.A. 1998. Model Selection and
Inference: A Practical Information-Theoretic Approach. New
York: Springer-Verlag, 353 pp.
CONGDON, J.D., TINKLE, D.W., BREITENBACH, G.L., AND VAN
LOBEN SELS, R.C. 1983. Nesting ecology and hatching success
in the turtle Emydoidea blandingii. Herpetologica 39:417–
429.
CONOVER, M.R. 2007. Predator-Prey Dynamics: The Role of
Olfaction. Boca Raton, FL: CRC Press, 248 pp.
COOPER, S.M. AND GINNETT, T.F. 2000. Potential effects of
supplemental feeding of deer on nest predation. Wildlife
Society Bulletin 28:660–666.
CRABTREE, R.L. AND WOLFE, M.L. 1988. Effects of alternate prey
on skunk predation of waterfowl nests. Wildlife Society
Bulletin 16:163–169.
ERNST, C.H. AND LOVICH, J.E. 2009. Turtles of the United States
and Canada, Second edition. Baltimore: Johns Hopkins
University Press, 827 pp.
GIBBONS, J.W. 1968. Population structure and survivorship in the
painted turtle Chrysemys picta. Copeia 1968:260–268.
GIBBS, J.P. AND SHRIVER, W.G. 2002. Estimating the effects of
road mortality on turtle populations. Conservation Biology
16:1647–1652.
HAMILTON, A.M., FREEDMAN, A.H., AND FRANZ, R. 2002. Effects
of deer feeders, habitat and sensory cues on predation rates on
artificial turtle nests. American Midland Naturalist 147:123–
134.
KOLBE, J.J. AND JANZEN, F.J. 2001. The influence of propagule
size and maternal nest-site selection on survival and
behaviour of neonate turtles. Functional Ecology 15:772–
781.
KOLBE, J.J. AND JANZEN, F.J. 2002a. Impact of nest-site selection
on nest success and nest temperature in natural and disturbed
habitats. Ecology 83:269–281.
KOLBE, J.J. AND JANZEN, F.J. 2002b. Spatial and temporal
dynamics of turtle nest predation: edge effects. Oikos 99:
538–544.
MILLER, J.R. AND HOBBS, N.T. 2000. Recreational trails, human
activity, and nest predation in lowland riparian areas.
Landscape and Urban Planning 50:227–236.
MILLER, S., KNIGHT, R., AND MILLER, C.K. 1998. Influence of
recreational trails on bird breeding communities. Ecological
Applications 8:162–169.
REFSNIDER, J.M. AND JANZEN, F.J. 2010. Putting eggs in one
basket: ecological and evolutionary hypotheses for variation
in oviposition-site choice. Annual Review of Ecology,
Evolution, and Systematics (in press).
135
SAS INSTITUTE. 2008. SAS User’s Guide: Statistics. Version 9.
Volume 1. Cary, NC: SAS Institute.
SCHLUTER, D. 1988. Estimating the form of natural selection on a
quantitative trait. Evolution 42:849–861.
SCHWANZ, L.E., SPENCER, R.-J., BOWDEN, R.M., AND JANZEN, F.J.
2010. Climate and predation dominate juvenile and adult
recruitment in a turtle with temperature-dependent sex
determination. Ecology (in press).
STEEN, D.A. AND GIBBS, J.P. 2004. Effects of roads on the
structure of freshwater turtle populations. Conservation
Biology 18:1143–1148.
STRICKLAND, J.T., COLBERT, P.L., AND JANZEN, F.J. 2010. An
experimental analysis of effects of markers and habitat
structure on predation of turtle nests. Journal of Herpetology
(in press).
TEMPLE, S.A. 1987. Predation on turtle nests increases near
ecological edges. Copeia 1987:250–252.
VALENZUELA, N. AND JANZEN, F.J. 2001. Nest-site philopatry and
the evolution of temperature-dependent sex determination.
Evolutionary Ecology Research 3:779–794.
VANDER LEE, B.A., LUTZ, R.S., HANSEEN, L.A., AND MATTHEWS,
N.E. 1999. Effects of supplemental prey, vegetation, and time
on success of artificial nests. Journal of Wildlife Management
63:1299–1305.
VICKERY, P.D., HUNTER, M.L., AND WELLS, J.V. 1993. Evidence
of incidental nest predation and its impacts on nests of
threatened grassland birds. Oikos 63:281–288.
Received: 20 August 2009
Revised and Accepted: 26 February 2010