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Evaluation of predator-exclusion cages used in turtle
conservation: cost analysis and effects on nest environment
and proxies of hatchling fitness
J. L. Riley
A
and J. D. Litzgus
A,B
A
Department of Biology, Laurentian University, 935 Ramsey Lake Road, Sudbury, Ontario, P3E 2C6, Canada.
B
Corresponding author. Email: jlitzgus@laurentian.ca
Abstract
Context. A main goal of conservation is to mitigate anthropogenic impacts on natural ecosystems, thus conservation tools
themselves should not negatively affect target species. Predator-exclusion cages are effectively used to reduce predation of
turtle nests; however, their effects on nest environment and developing hatchlings have not been examined.
Aims. Our study had the following four goals: (1) to examine effects of cages on the nest environment, (2) determine
whether nest caging affects proxies for hatchling fitness, (3) evaluate whether nest predators preferentially interact with
certain cage types, and (4) assess the cost-effectiveness of different nest caging designs.
Methods. In 2010 and 2011 in Algonquin Provincial Park, Ontario, painted turtle (Chrysemys picta;n= 93) and snapping
turtle (Chelydra serpentina;n= 91) nests were assigned to one of three treatments (wooden-sided cages, above- and below-
ground wire cages) or a control (no nest cage) and outfitted with a data logger to record incubation temperature. After
emergence, hatching success and proxies of hatchling fitness were measured.
Key results. Nest temperature, hatching success, frequency of hatchling deformities and locomotor performance did not
differ among cage treatments. However, hatchling body condition differed among treatments; wooden-sided and below-
ground cages had the most positive influence on body condition in painted and snapping turtles, respectively. Predator
interactions did not differ among treatments, and wooden-sided cages were the most inexpensive to construct.
Conclusions. Nest cages did not alter the nest environment from natural conditions but did alter hatchling body condition,
and nest caging affected species differently.
Implications. Nest cages are known to reduce nest depredation, and our data indicated that, in general, nest cages also do
not affect the nest environment or proxies for hatchling fitness. Thus, our findings indicated that cages are effective
conservation tools that do not present secondary deleterious effects on potential recruitment.
Received 16 May 2013, accepted 4 October 2013, published online 7 November 2013
Introduction
An increasingly important priority in the field of conservation
biology is the mitigation of human impacts on natural ecosystems.
Thus, conservation techniques themselves should not incur
negative, secondary impacts on target species (Frazer 1992).
A global threat to marine and freshwater turtles and tortoises is
increased nest predation as a result of subsidised predators.
Predators of turtle eggs (e.g. raccoons, skunks, foxes) increase
in abundance because of an increase in food resources associated
with human presence, which in turn causes nest predation to
occur at higher-than-natural levels (Christiansen and Gallaway
1984; Garber and Burger 1995; Mitchell and Klemens 2000;
Engeman et al.2003; Barton and Roth 2008; Kurz et al.2011;
Spotila 2011; Smith et al.2013). In addition, decreases in
populations of top predators in urban areas (e.g. wolves, large
cats) have increased the numbers of mesopredators, again leading
to increases in depredation of turtle eggs (Prugh et al.2009;
Ritchie and Johnson 2009). In some turtle populations, subsidised
mesopredators annually depredate 100% of nests, resulting in
chronic prevention of recruitment (Spinks et al.2003; Fordham
et al.2008). Substantial, repeated reductions in recruitment (e.g.
50% or more decrease in egg survival) have been found to
exacerbate population declines (Crouse et al.1987; Crowder
et al.1994; Heppel 1997; Tomillo et al.2008; Reed et al.2009).
The conservation tool used worldwide to eliminate nest predation
and promote recruitment is nest caging. Nest caging reduces nest
predation from as high as 100% depredation of nests without
cages to as low as 0% depredation of nests with cages (Addiston
1997; Ratnaswamy et al.1997; Yerli et al.1997; Gillingwater
2001; Engeman et al.2006; Kornaraki et al.2006; Kurz et al.
2011; Perez-Heydrich et al.2012; Smith et al.2013). This tool has
been in use since the 1960s (Breckenridge 1960), and specific
methods vary considerably among studies, many of which are
unpublished stewardship projects. Shortcomings of the technique
have been noted, namely, wire cages can entrap hatchlings
(Adamany et al.1997), wire cages alter the magnetic field
CSIRO PUBLISHING
Wildlife Research
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around the nest, which may affect sea turtle orientation and
navigation (Irwin et al.2004), and cages with materials above
ground level may alter the nest environment (e.g. shading which
would reduce incubation temperature; Breckenridge 1960;
Rahman and Burke 2010). Female turtles select nest sites on
the basis of environmental characteristics that maximise hatching
success (Wilson 1998; Refsnider and Janzen 2010). Evidence that
nest caging may alter those characteristics suggests that this
technique requires evaluation.
Nest environment (e.g. incubation temperature, soil moisture)
greatly influences hatchling performance and morphology.
Reduced incubation temperature results in a decline in
hatching success (Correa-H et al.2010; Garrett et al.2010). In
northern temperate regions (e.g. Ontario, Canada), if incubation
temperatures are reduced, turtle embryos may not complete
development or emerge from the nest cavity before the onset
of cool fall temperatures (Yntema 1968; Choo and Chou 1987;
Bobyn and Brooks 1994; Du and Ji 2003). In addition, incubation
may be extended into a time period when habitat conditions are
unfavourable (Bobyn and Brooks 1994; Matsuzawa et al.
2002). Furthermore, embryos exposed to low temperatures
during incubation have reduced body condition, a higher
frequency of deformities and reduced locomotor performance
(Díaz-Paniagua et al.1997; Packard et al.1999; Hewavisenthi
and Parmenter 2001; Steyermark and Spotila 2001; Reece et al.
2002; Du and Ji 2003; Booth et al.2004). Many turtle species
exhibit temperature-dependent sex determination (TSD), and
altered nest temperatures could result in skewed sex ratios
(Schwarzkopf and Brooks 1985; Janzen and Paukstis 1991;
Hanson et al.1998; Wibbels 2003), in turn leading to reduced
population viability (Steen and Gibbs 2004). More broadly,
hatchling survival, growth rates, behaviours and habitat
selection have all been related to incubation temperature
(McKnight and Gutzke 1993;O’Steen 1998; Rhen and Lang
1999;Booth et al.2004). In general, a substantial portion
of a turtle’s individual characteristics are determined by the
environment during embryogenesis.
The goal of the research presented here was to evaluate nest
caging types in terms of their impacts on nest environment,
proxies for hatchling fitness, predator attraction and logistical
considerations. The following three types of nest cages currently
used in the recovery of at-risk turtles were evaluated: above- and
below-ground hardware cloth cages, and wooden-sided cages.
Data were also collected from natural nests (e.g. non-caged
control nests). The first objective of the study was to compare
the effect different nest cage types may have on the environment
of the nest. We tested the hypothesis that if nest cage materials
block solar radiation, then temperature within the nest cavity
of above-ground and wooden-sided cages will be reduced. The
second objective was to determine the effect different nest cages
may have on hatching success, incubation duration, hatchling
body condition and performance. Following the prediction from
objective one, if temperature within the nest cavity is reduced,
this will have negative effects on nest success and hatchling
fitness. We tested the prediction that above-ground and wooden-
sided cages would experience lower hatching success and longer
incubation durations. Also, we predicted that above-ground and
wooden-sided cages would have a negative effect on proxies of
hatchling fitness, measured as a higher frequency of deformities
(Mast and Carr 1989; Türkozan et al.2001), reduced body
condition (Shine et al.2001) and reduced locomotor
performance (Freedberg et al.2004; Delmas et al.2007). Nest
predators may use research markers as visual cues for predation
(Burke et al.2005; Rollinson and Brooks 2007; Spotila
2011); thus, the third objective was to determine whether
predators preferentially interacted with, and depredated nests
with protective cages. If nest cages were used as visual cues,
then we predicted that predators would preferentially interact
with, and depredate above-ground and wooden-sided nest cages.
As conservation initiatives are often constrained by funding, the
final objective of our study was to perform a cost analysis of each
nest cage type.
Methods
Study area
The study took place in Algonquin Provincial Park, Ontario,
Canada, near the Wildlife Research Station (WRS; 45350N,
78300W). Elevations on the western side of Algonquin Park
(370–570 m above sea level) are higher than the surrounding
landscape and the area experiences a colder and wetter climate as a
result (Ontario Ministry of Natural Resources 1998). This climate
is reflective of the northern range limits of both turtle species
studied. The study area is within the Algonquin–Lake Nipissing
ecoregion, and is a rugged landscape underlain by Precambrian
Shield outcrops (Ontario Ministry of Natural Resources 1998).
Forest cover dominates, including predominantly mixed upland
forests of sugar maple (Acer saccharum), yellow birch (Betula
alleghaniensis) and eastern hemlock (Tsuga canadensis). Field
sampling was concentrated in two study sites, namely, WRS and
Arowhon. Nesting habitat in the WRS site varies from natural
sand dunes to gravel embankments along access roads and
Highway 60. The Arowhon site main nesting area is the sand
and gravel embankment of a public hiking trail (Schwarzkopf and
Brooks 1985).
Snapping and painted turtle populations are substantial at the
study sites, and nesting has been consistently documented over
the past 35+ years (R. J. Brooks, University of Guelph, unpubl.
data). By using these two relatively common species, we could
achieve large sample sizes and robust statistical analyses, leading
to findings about nest caging applicable to turtle species-at-risk.
Examining two species with different nest characteristics,
namely, shallow nest with a small number of eggs (painted
turtles) vs deep nest with a large number of eggs (snapping
turtles), allowed us to capture variation among species.
Field methodology
Nest-site monitoring occurred from 20 May to 20 June 2010, and
5 June to 4 July 2011. Nest monitoring commenced when females
of either species started to congregate in aquatic habitats adjacent
to nest sites (i.e. staging), and/or terrestrial nest searching
behaviour was observed. Nest sites were monitored visually by
researchers from dawn (~0500 hours) to ~1000hours, and in the
afternoon from just before dusk (~1700 hours) until after dark, as
long as nesting activity was occurring. This timing captured
peak nesting for snapping and painted turtles (Ernst and
Lovich 2009). Nest monitoring ceased when 3 days elapsed
continuously without any observations of nesting activity.
BWildlife Research J. L. Riley and J. D. Litzgus
Nests were excavated after females completed oviposition
and covering of their nests. Nest locations were marked with
metal stakes and flagging tape. Eggs were removed, and placed
in plastic bins lined with moistened vermiculite. As eggs were
removed, they were numbered using a pencil, to ensure that they
were returned to the nest cavity in the same order and orientation
as they were found. Depth to the top and bottom of the nest
cavity was measured to the nearest 0.1 cm by using a ruler.
After excavation, nest cavities were filled with soil removed
during egg retrieval, to reduce desiccation of the nest chamber.
Eggs were transported back to the WRS laboratory, where data
were collected for the long-term study. Eggs were returned to
the nest cavity within 24 h post-oviposition, before the vitteline
membrane adhered to the inner shell surface to form a ‘white
spot’on the egg (Yntema 1968; Rafferty and Reina 2012),
ensuring no trauma to developing embryos (Samson et al.2007).
Each nest was randomly assigned to one of the treatments
(Table 1). In 2010, there were two treatments, above- and below-
ground hardware cloth cages, and a control (no cage). In 2011, an
additional treatment, namely wooden-sided cages, was added.
The cages were all open-bottomed cubes. The above-ground cage
was made with 1-cm-mesh hardware cloth; dimensions were
30 30 40 cm, with 8-cm flaps, and they were installed with
20 cm above and 20 cm below ground surface (Fig. 1; Addiston
1997; Irwin et al.2004). Below-ground cages were also made of
1-cm hardware cloth; dimensions were 30 30 20 cm and did
not have any flaps, and they were installed so that the top of the
cage was just below ground level (Fig. 1; Hughes and Brooks
2006; Bolton et al.2008). The wooden-sided cages consisted of
a wooden square frame (made of boards 14 3.8 35 cm) with a
1-cm hardware-mesh top. The dimensions were 35 35 9 cm,
and the cages were installed over the top of the nest, with none of
the cage extending below the ground, and with either rocks or
stakes holding the cage securely against the soil (Fig. 1; Standing
et al.1999). Eggs were reburied in the original nest cavity, at
the original depths and order, with a temperature data logger in
the centre of the clutch. The temperature data loggers were
either a waterproofed iButton
®
(accuracy of 1C or 0.5C;
Thermochron DS1921G; Dallas Semiconductor, Sunnyvale,
CA, USA), or a HOBO StowAway
®
(accuracy of 0.2C;
TidbiT TBI32-05+37; Onset Computer Corporation, Bourne,
CA, USA). Temperature readings from data loggers of
different types and with and without waterproofing did not
differ (F
3,2480
= 2.01, P= 0.94; Roznik and Alford 2012). Data
loggers recorded temperature hourly. Cages were installed
immediately after egg reburial and data-logger deployment.
For the control nests, a second data logger was buried beside
the nest at the same depth as the logger within the nest cavity.
This was done so that if a control nest was depredated and the
‘in-nest’data logger was consumed or excavated by the predator,
incubation-temperature data would still be available. In late
August 2010 and 2011, close to the estimated date of
hatchling emergence (and after embryogenesis), above-ground
cages were installed on the control nests so that emerging
hatchlings could be collected for measurement and fitness tests.
Nest environmental variables were measured for all cage
treatments. Vegetation cover was estimated by placing a 1-m
2
quadrat on the ground with the nest in the centre, and the
percentage of bare ground, herbaceous and woody plants, and
leaf litter were visually estimated (Wilson 1998). In 2010 and
2011, vegetation cover was sampled monthly and bi-weekly,
respectively, post-egg reburial until hatchling emergence.
Additionally, on 16 August 2011, soil moisture (%) was
measured at a depth of 10 cm within the area enclosed by the
nest cage, or for control nests, beside the stake marking the
nest site. Soil moisture was measured using a VG-METER-
200 (Vegetronix, Bluffdale, UT, USA).
In 2010 and 2011, predator interactions with nest cages
were recorded daily throughout nesting and hatching seasons.
Outside of those time periods in 2010, nests were surveyed
opportunistically. In 2011, nests were surveyed for predator
interactions once per week. A ‘predator interaction’was
recorded when substrate was cleared away from the nest cage,
and/or the cage was dug up. After recording a predator interaction,
soil was replaced around the nest so that multiple interaction
events could be recorded. If a nest was found with the eggs dug up
and/or eaten, the nest was recorded as depredated. If tracks and
scat were discernible, the predator species was identified and
recorded. Additionally, four trail cameras (119456C; Bushnell
Corporation, Overland Park, KS, USA) were set up from 1 July to
1 October 2011 at four different locations to capture interactions
of predators with nest cages.
Daily monitoring of nests began just before the estimated
period of hatchling emergence. The emergence time for nests was
estimated using incubation durations reported in literature for
snapping (63–104 days) and painted turtles (89–99 days; Ernst
and Lovich 2009). The first nests of both snapping and painted
turtles emerged on 25 August in 2010 and, in 2011, on 27 August
for painted turtles and 1 September for snapping turtles. Once a
nest emerged, all hatchlings and unhatched eggs were collected
and transported to the WRS laboratory for processing. Hatchling
carapace and plastron lengths were measured to the nearest
0.01 mm by using digital calipers (3148, Traceable Digital
Calipers, Control Co., Friendswood, TX, USA). Hatchling
mass was measured to the nearest 0.1 g by using a digital scale
(SP202, Scout Pro, Ohaus Corporation, Pine Brook, NJ, USA).
Any deformities (e.g. curly tails, additional scutes) were recorded.
Deformities were considered to be any deviation from the normal
body plan (Ernst and Lovich 2009) that did not appear to be
caused by injury (Davy and Murphy 2009).
Each hatchling underwent a righting test. Each hatchling was
placed on its carapace on a cloth-covered board (30 15 cm) and
Table 1. Number of nests per treatment and number of hatchlings per
treatment (in parentheses, italic font) sampled during the 2010 and 2011
field seasons in Algonquin Park, Ontario, Canada
For the control treatment, the first number before the comma represents the
number of nests sampled for both environmental and hatchling data, and
the number after the comma represents the number of nests sampled only for
environmental data
Treatment Chrysemys picta Chelydra serpentina
2010 2011 2010 2011
Control (no cage) 9, 5 (31) 12, 6 (43)8,6(193) 12, 3 (288)
Below-ground cage 12 (63)13(56)12(291)12(352)
Above-ground cage 12 (29)12(61)12(294)14(312)
Wooden-sided cage –12 (66)–12 (272)
Total 38 (123)55(226)38(778)53(1224)
Effects of predator-exclusion cages on turtle nests Wildlife Research C
attempts to flip over onto its plastron were observed for 15 min.
The following two variables were timed to the nearest 0.01 s by
using a digital stopwatch: (1) latency period (LP), the time from
placement on carapace until the first righting attempt; and
(2) righting period (RP), the time from the first righting
attempt until successful righting (Freedberg et al.2004;
Delmas et al.2007; Rasmussen and Litzgus 2010). Each trial
was recorded with a digital camera (Photosmart R742, Hewlett-
Packard Development Co., Mississauga, ON, USA), and LP
and RP were confirmed from the recordings. The number of
hatchlings that failed to right themselves within 15 min was
compared among treatments; these hatchlings were removed
from the comparison of RP among treatments. A turtle that
cannot quickly right itself is more likely to be depredated, or
to succumb to desiccation and drowning (Finkler and Claussen
1997). Thus, performance in righting tests is thought to reflect a
hatchling’s future survival, and therefore was used as a proxy
for fitness (Freedberg et al.2004; Delmas et al.2007). After data
collection, hatchlings were released at their nests within 24 h. The
unhatched eggs were candled to assess fertility (Yntema 1964).
Emergence ceased on 30 September 2010 and 28 September
2011. Once daily mean air temperature dropped below 5C for
three consecutive days, any remaining nests were dug up to assess
hatching success. In 2010, unemerged nests were dug up from 1 to
4 October, and in 2011 from 2 to 7 October. Any hatchlings were
processed as described above.
We undertook a cost analysis of each caging design. First, we
calculated the monetary cost of equipment for each design, and
second, we calculated the effort (salary cost) to make and install
each cage by a technician. Time (to nearest min) was recorded
as technicians constructed and installed cages. The times for all
actions were then averaged, and multiplied by the technician’s
salary cost (CAN$10.25 per h, the minimum wage in Ontario,
Canada) to estimate the effort per cage design.
Analyses
Nest environmental variables, except temperature, were averaged
for each treatment. Because these data were non-normal, mean
soil moisture and vegetation cover were compared among
(a)
(b)
(c)(d)
Fig. 1. Three nest-cage types were tested. In 2010, nests were randomly assigned to (a) below-ground
cages, (b) above-ground cages (shown before and post-installation from left to right), or (d) uncaged
nests (controls). In 2011, the 2010 treatments were repeated with the addition of (c) wooden-sided nest
cages.
DWildlife Research J. L. Riley and J. D. Litzgus
treatments separately for each turtle species, using a non-
parametric Kruskal–Wallis ANOVA test. Depth to the bottom
of the nest cavity was compared between species using an
ANOVA.
The temperature data were extracted from data loggers, and
data from ‘in-nest’data loggers were preferentially used for the
control treatments. No difference was found in temperature
between ‘in-nest’and ‘out-of-nest’data loggers (2011 data:
t
44
= 2.02, P= 0.89), so the ‘out-of-nest’temperature data were
used when a control nest was predated.
Temperature data were analysed three ways. (1) Mean nest
temperature from the date of the last nest reburied to the first
nest emerged (a 44- and 57-day period in 2010 and 2011,
respectively), and daily temperature variance during this time
period, were calculated for each nest. Mean daily temperature
variance describes daily temperature fluctuations above and
below mean nest temperature (Paitz et al.2010; Neuwald and
Valenzuela 2011), and is known to affect hatchling development
(Schwarzkopf and Brooks 1985; Doody 1999; Ashmore and
Janzen 2003; Du and Ji 2003; Mullins and Janzen 2006; Les
et al.2007; Paitz et al.2010). (2) Mean temperature for each
third of incubation (Packard and Packard 1998), and daily mean
temperature and mean temperature variance for the second third
of incubation, the time period when sex is determined (Mahmoud
et al.1973; Yntema 1979; Bull and Vogt 1981; Bull 1985; Paitz
et al.2010; Neuwald and Valenzuela 2011), were calculated.
(3) Heat units (degree days, D) were calculated for each nest
by using the hourly trapezoid method (Holt 2000). Degree days
represent the number of heat units over a 24-h period above a
threshold temperature (T
o
). Below T
o
, no development occurs,
but above it, heat units stimulate development (Holt 2000). The
threshold temperature is 14C for painted turtles (Les et al.
2007), and 20C for snapping turtles (Holt 2000). We used
hourly temperatures to capture fluctuations in temperature that
affect development. The hourly trapezoid method uses hourly
temperatures (T
0
,T
1
,T
2
,... T
23
) to calculate heat units (HU)
above a threshold temperature (T
o
):
HU ¼ ½ððT0þT1Þ=2ÞþððT1þT2Þ=2Þ
þþððT22 þT23Þ=2Þ=ð24 ToÞ
Temperature, temperature variance, temperatures for each
third of incubation, and heat units were compared among
treatments using ANOVAs that also included the additional
factors of species and year as necessary.
Hatching success (%) for each nest was calculated as the
number of live hatchlings divided by the number of eggs laid.
Hatching success was compared among treatments, species
and years by using a Kruskal–Wallis ANOVA. Incubation
duration was the number of days between oviposition and
hatchling emergence for each nest and was compared among
treatments using an ANOVA that included the additional factors
of species and year. Deformities were quantified as the proportion
of deformed turtles out of the number of hatchlings in a clutch
(Davy and Murphy 2009). Proportion of deformed turtles in
each clutch was transformed using an arcsine-square-root
transformation to ensure normality (Gotelli and Ellison 2004).
Mean number of deformities per turtle in each clutch was also
calculated (de Solla et al.2008). To control for the random effect
of mother’s identity, a linear mixed-effects model (LMEM) using
a restricted maximum likelihood estimation of variance was used
to examine whether deformities (proportion of hatchlings with
deformities in each clutch, and mean number of deformities per
hatchling per clutch) varied among treatments. In this model,
additional fixed factors of species and year were included. Body
condition was tested separately for each species using a LMEM to
compare mass against the fixed effects of treatment and carapace
length, and the random effect of clutch nested in mother’s identity
(García-Berthou 2001; Litzgus et al.2008; Rasmussen and
Litzgus 2010). The number of hatchlings that failed to right
themselves within 15 min was compared among treatments
using a Pearson’s Chi-squared test of association. Performance
variables (LP and RP) were transformed using log (y+ 1) to ensure
normality. LP and RP were tested separately for each species
among treatments using a LMEM that included the fixed effect of
processing temperature (room temperature during righting tests),
which is linearly related to ectotherm performance (Hutchison
et al.1966), and the random effect of clutch nested in mother’s
identity (to control for genetic effects).
Pearson’s Chi-squared tests of association were used to test
whether count data from predation interactions and depredation
events differed among treatments. A one-way ANOVA was used
to test whether installation time (s) differed among treatments.
In all statistical tests, assumptions of normality and
heterogeneity of variance were verified. Measures were
transformed for normality as needed. An a posteriori Tukey
HSD test, which adjusted for multiple comparisons, was used
to identify differences among sample means when significant
differences were found among treatments (Logan 2010). If a
significant interaction was found in models with multiple fixed
factors, it was reported, and if no significant interaction was
found, only main effects were tested and reported. All summary
data are reported as the mean 1 standard error. The significance
level of a=0.05 was used for all statistical tests. Statistical
analyses were performed using R (R Foundation for Statistical
Computing, Vienna, Austria).
Results
Nest environment
Mean soil moisture (%) in the nests of painted and snapping
turtles did not differ among treatments (Table 2). For painted
turtle nests, percentage bare ground, leaf litter and herbaceous
plants did not differ among treatments (Table 2). Mean percentage
woody plants differed among treatments; nests with wooden-
sided cages had a greater percentage of woody plants than did
those in other treatments (Table 2). None of the vegetation
characters differed among treatments for snapping turtle nests
(Table 2). Nest depth differed between species (F
1,177
= 726.1,
P<0.01); snapping turtles had deeper nests (20.7 0.4 cm) than
painted turtles (9.6 0.1 cm).
Nest thermal environment
Mean incubation temperature (C) did not differ among cage
treatments (F
3,155
= 1.05, P= 0.37) or between species
(F
1,155
= 0.01, P= 0.91), but differed between years
(F
1,155
= 22.17, P<0.01; Tables 3,4). Mean daily temperature
variance in nests of painted turtles varied more than in those of
Effects of predator-exclusion cages on turtle nests Wildlife Research E
snapping turtles (F
1,159
= 203.93, P<0.01; Tables 3,4). Mean
daily temperature variance did not differ among treatments for
painted turtles (F
3,75
= 1.42, P= 0.24; Table 3), but did differ
among treatments for snapping turtles (F
3,81
= 3.42, P= 0.02;
Table 4). Snapping turtle nests with wooden-sided cages
experienced less variation than did nests with below-ground
cages (P= 0.02 for the comparison between wooden-sided and
below-ground cages, P>0.05 for all other cases; Table 4).
Mean temperature in each third of incubation did not differ
among treatments (F
3,67
= 1.09, P= 0.36; F
3,67
= 1.98, P= 0.13;
F
3,67
= 2.36, P= 0.08, respectively), or between species
(F
1,67
= 1.82, P= 0.18; F
1,67
= 0.01, P= 0.94; F
1,67
= 0.78,
P= 0.38, respectively), but differed between years
(F
1,67
= 39.14, P<0.01; F
1,67
= 13.99, P<0.01; F
1,67
= 18.17,
P<0.01, respectively; Tables 3,4).
In the second third of incubation, mean daily temperature
did not differ among treatments (F
3,67
= 2.09, P= 0.11) or
between species (F
1,67
= 0.003, P= 0.95), but differed
between years (F
1,67
= 12.76, P<0.01; Tables 3,4). For the
same period, mean daily temperature variance did not differ
among treatments (F
3,67
= 1.30, P= 0.28) or between years
(F
1,67
= 1.70, P= 0.20), but differed between species
(F
1,67
= 300.45, P<0.01); mean daily temperature variance
was greatest in painted turtle nests (Tables 3,4).
Heat units (D) were tested separately for each species,
because the threshold temperature differs between them. Mean
heat units did not differ among treatments or between years
for painted turtles (F
3,13
= 0.51, P= 0.68; F
1,13
= 0.15, P= 0.71,
respectively; Table 3) or snapping turtles (F
3,47
= 0.66, P= 0.58;
F
1,49
= 2.36, P= 0.13, respectively; Table 4).
Clutch and hatchling characteristics
Mean incubation duration did not differ among treatments
(F
3,81
= 0.44, P= 0.73), or between species (F
1,81
= 0.74,
P= 0.39), but it was shorter in 2011 than in 2010 (F
1,81
= 4.27,
P= 0.04; Tables 5,6). Hatching success did not differ among
treatments in painted (H
3
= 5.25, P= 0.15; Table 5) or snapping
turtles (H
3
= 2.93, P= 0.40; Table 6).
Mean proportion of deformed turtles in each clutch did not
differ among treatments (F
3,130
= 1.56, P= 0.20), between species
(F
1,130
= 0.28, P= 0.60) or between years (F
1,130
= 2.25, P= 0.14;
Tables 5,6). Mean number of deformities per hatchling in each
clutch also did not differ among treatments (F
3,131
= 2.56,
P= 0.06) or between species (F
1,131
= 3.15, P= 0.08), but there
were on average more deformities per hatchling in 2011 than in
2010 (F
1,131
= 5.11, P= 0.03; Tables 5,6).
Body condition of painted turtles differed among treatments
(F
3,345
= 3.09, P= 0.03). Mass was greater at all carapace lengths
measured for hatchlings from wooden-sided cages. For body
condition of snapping turtles, a significant interaction was found
between treatment and carapace length (F
3,1988
= 107.09,
P<0.01). Mass was slightly greater at all carapace lengths
measured for hatchlings from below-ground cages than that for
those from the control and above-ground cages. Hatchlings from
above-ground cages had the lowest mass at carapace lengths less
than 27 mm. At carapace lengths less than ~28 mm, hatchlings
from wooden-sided cages had the greatest mass, but at carapace
lengths greater than ~28 mm, they had the lowest masses.
Table 2. Summary of soil moisture and vegetation types quantified in 1-m
2
quadrats centred on turtle nests in four nest-caging treatments
Data are means s.e. (%). Number of nests (n) is provided for each treatment. Test statistics from the Kruskal–Wallis ANOVA test (H), degrees of freedom, and P-values are given for each nest characteristic.
Significant test results are indicated in bold font. Data were analysed separately for each species to determine whether nest-environment characteristics differed among nest-cage treatments
Nest-environment Chrysemys picta Chelydra serpentina
characteristics Above-
ground cages
(n= 24)
Below-
ground cages
(n= 24)
Wooden-
sided cages
(n= 12)
No cage
(n= 31)
Test statistics Above-
ground cages
(n= 25)
Below-
ground cages
(n= 24)
Wooden-
sided cages
(n= 12)
No cage
(n= 29)
Test statistics
Soil moisture 9.2 ± 1.0 6.1 ± 0.5 6.7± 0.8 8.5 ± 1.1 H
3
= 7.04, P= 0.07 5.3 ± 0.6 6.9 ± 1.0 6.4± 1.5 8.1 ± 1.8 H
3
= 3.35, P= 0.34
Bare ground 77.1 ± 2.4 81.1 ± 3.3 67.9 ± 5.2 70.5 ± 3.3 H
3
= 7.74, P= 0.06 87.9 ± 2.7 86.3 ± 2.4 89.2 ± 2.6 84.0 ± 2.6 H
3
= 1.13, P= 0.77
Herbaceous plants 13.2 ± 1.9 12.2 ± 2.6 13.6 ± 3.7 17.8 ± 2.6 H
3
= 2.93, P= 0.40 7.5 ± 1.5 7.8 ± 1.7 6.1± 1.8 12.6 ± 2.3 H
3
= 0.43, P= 0.94
Woody plants 6.5 ± 1.3 3.6 ± 0.9 13.6± 3.7 7.0 ± 1.4 H
3
= 8.24, P= 0.04 1.3 ± 0.6 1.8± 0.7 3.2 ± 1.9 1.3 ± 0.5 H
3
= 1.50, P= 0.68
Leaf litter 3.2 ± 0.5 3.1 ± 0.9 6.8± 2.2 4.3 ± 0.8 H
3
= 5.74, P= 0.13 3.3 ± 1.7 4.0 ± 1.8 1.6± 0.5 2.1 ± 0.6 H
3
= 3.37, P= 0.34
FWildlife Research J. L. Riley and J. D. Litzgus
The number of hatchlings that failed to right themselves in
15 min did not differ among treatments for painted (c
23
= 0.52,
P= 0.92; Table 5) or snapping turtles (c
23
= 3.60, P= 0.31;
Table 6). LP and RP of painted turtles did not differ among
treatments (F
3,327
= 1.79, P= 0.15; F
3,326
= 0.17, P= 0.92;
Table 5), and LP and RP of snapping turtles did not differ
among treatments (F
3,1853
= 1.81, P= 0.14; F
3,1850
= 2.08,
P= 0.10; Table 6). A significant interaction between treatment
and processing temperature was found for snapping turtle RP
(F
3,1850
= 2.93, P= 0.03). Hatchlings from above-ground cages
had the slowest RP across all processing temperatures. The slope
of RP versus processing temperature was similar for the wooden-
sided and control treatment; over most processing temperatures,
hatchlings from wooden-sided and control nests had the fastest
RP. However, RP did not vary by more than half a second between
any treatments.
Predators and nest cages
Over the course of incubation, the number of predator interactions
with above-ground cages was 14, with below-ground cages 16,
and with wooden-sided cages it was 2. The number of caged
nests with which predators interacted did not differ among
treatments (c
22
= 0.06, P= 0.97). The number of successful
depredation events was 3, 1 and 3 for above-ground, below-
ground and wooden-sided cages, respectively. The number of
Table 3. Summary of Chrysemys picta nest-temperature data
Data are means s.e. and sample sizes (n= number of nests) are given in parentheses
Temperature variable Nest-cage treatment
Above-ground cages Below-ground cages Wooden-sided cages Control (no cage)
2010 2011 2010 2011 2010 2011 2010 2011
Summer hourly temperature (C) 23.8 ± 0.15
(n= 11)
24.8 ± 0.26
(n=9)
23.7 ± 0.45
(n=9)
25.3 ± 0.25
(n=9)
–24.4 ± 0.31
(n= 12)
23.9 ± 0.24
(n= 14)
24.3 ± 0.30
(n= 16)
Heat units (D) 803.4
(n=1)
815.8 ± 0.5
(n=4)
–819.6 ± 0.3
(n=2)
–781.8 ± 0.6
(n=4)
849.6 ± 0.3
(n=5)
812.9 ± 0.02
(n=2)
Temperature variance (C) 15.0 ± 3.1
(n= 11)
15.7 ± 1.6
(n=9)
15.6 ± 2.0
(n=9)
19.2 ± 1.2
(n=9)
–15.0 ± 1.9
(n= 12)
15.9 ± 1.5
(n= 14)
20.8 ± 1.5
(n= 16)
First third of incubation
hourly temperature (C)
20.3
(n=1)
22.7 ± 0.9
(n=4)
–22.2 ± 0.5
(n=2)
–22.5 ± 0.6
(n=4)
21.9 ± 0.2
(n=5)
22.2 ± 0.2
(n=2)
Second third of incubation
hourly temperature (C)
24.4
(n=1)
25.7 ± 0.6
(n=4)
–27.5 ± 0.5
(n=2)
–25.4 ± 0.7
(n=4)
24.8 ± 0.3
(n=5)
25.4 ± 0.06
(n=2)
Final third of incubation
hourly temperature (C)
23.0
(n=1)
21.0 ± 0.6
(n=4)
–22.5 ± 0.02
(n=2)
–20.4 ± 1.1
(n=4)
22.8 ± 0.3
(n=5)
20.2 ± 0.3
(n=2)
Second third of incubation
daily temperature (C)
24.4
(n=1)
25.7 ± 0.6
(n=4)
–27.5 ± 0.5
(n=2)
–25.4 ± 0.7
(n=4)
24.8 ± 0.3
(n=5)
25.4 ± 0.06
(n=2)
Second third of incubation
temperature variance (C)
22.6
(n=1)
20.4 ± 2.1
(n=4)
–21.1 ± 5.4
(n=2)
–20.39 ± 3.8
(n=4)
19.0 ± 2.9
(n=5)
19.9 ± 2.4
(n=2)
Table 4. Summary of Chelydra serpentina nest temperature data
Data are means s.e. and sample sizes (n= number of nests) are given in parentheses
Temperature variable Nest-cage treatment
Above-ground cages Below-ground cages Wooden-sided cages Control (no cage)
2010 2011 2010 2011 2010 2011 2010 2011
Summer hourly temperature (C) 23.5 ± 0.3
(n= 12)
24.7 ± 0.4
(n=9)
24.1 ± 0.2
(n= 11)
25.0 ± 0.3
(n= 10)
–24.2 ± 0.4
(n= 11)
24.2 ± 0.2
(n= 14)
24.5 ± 0.3
(n= 14)
Heat units (D) 291.2 ± 0.2
(n=6)
322.1 ± 0.3
(n=8)
296.6 ± 0.2
(n=8)
326.6 ± 0.3
(n= 10)
–310.5 ± 0.3
(n=7)
284.2 ± 0.1
(n=5)
292.0 ± 0.3
(n= 10)
Temperature variance (C) 4.1 ± 0.4
(n= 12)
4.6 ± 0.6
(n=9)
6.3 ± 1.7
(n= 11)
6.7 ± 1.0
(n= 10)
–3.1 ± 0.5
(n= 11)
6.0 ± 1.0
(n= 14)
5.1 ± 0.7
(n= 14)
First third of incubation
hourly temperature (C)
21.5 ± 0.4
(n=7)
23.0 ± 0.3
(n=8)
21.1 ± 0.2
(n=8)
23.1 ± 0.2
(n= 10)
–22.9 ± 0.4
(n=7)
21.8 ± 0.4
(n=5)
23.0 ± 0.3
(n= 10)
Second third of incubation
hourly temperature (C)
24.6 ± 0.2
(n=7)
26.4 ± 0.5
(n=8)
25.0 ± 0.3
(n=8)
26.3 ± 0.5
(n= 10)
–26.1 ± 0.4
(n=7)
24.6 ± 0.2
(n=5)
25.3 ± 0.6
(n= 10)
Final third of incubation
hourly temperature (C)
22.4 ± 0.6
(n=7)
21.4 ± 0.6
(n=8)
23.1 ± 0.3
(n=8)
20.9 ± 0.5
(n= 10)
–21.1 ± 0.5
(n=7)
21.3 ± 0.6
(n=5)
20.2 ± 0.7
(n= 10)
Second third of incubation
daily temperature (C)
24.6 ± 0.2
(n=7)
26.4 ± 0.5
(n=8)
25.1 ± 0.4
(n=8)
26.3 ± 0.5
(n= 10)
–26.1 ± 0.4
(n=7)
24.6 ± 0.2
(n=5)
25.3 ± 0.6
(n= 10)
Second third of incubation
temperature variance (C)
4.1 ± 0.6
(n=7)
4.7 ± 0.4
(n=8)
4.4 ± 1.0
(n=4)
6.7 ± 2.7
(n=2)
–2.7 ± 0.5
(n=7)
3.4 ± 0.4
(n=5)
4.6 ± 0.7
(n= 10)
Effects of predator-exclusion cages on turtle nests Wildlife Research G
nests successfully depredated did not differ among treatments
(c
22
= 0.22, P=0.90). The number of nests successfully
depredated after being interacted with by a predator one or
more times was 1 for above-ground cages, 0 for below-ground
cages, and 1 for wooden-sided cages.
Images of predators investigating the nest cages (either
sniffing or looking at the cage) were captured 23 times by the
trail cameras, and included Vulpes vulpes,Canis lycaon and
Corvus corax. Predators interacting with nest cages (e.g.
digging) were captured 18 times by the cameras and included
V. vulpes and C. lycaon; these interactions were verified by visual
inspections of the nests.
Cost analysis of nest-cage designs
Wooden-sided cages were made of the least expensive materials,
and above-ground cages required the most expensive materials
(Table 7). Construction time was shortest for wooden-sided cages
and longest for above-ground cages (Table 7). Installation time
did not differ among cage types (F
2,24
= 2.11, P= 0.14;
Table 5. Summary of Chrysemys picta clutch and hatchling data
Data are means s.e. For the first four variables (1–4), samples size (n) represents the number of nests, and for the last three variables (5–7), nrepresents the number
of hatchlings. If data were analysed between years, means are shown separated by commas, and in some instances, year data were pooled. LP, latency period; RP,
righting period
Clutch and hatchling variable Nest-cage treatment
Above-ground cages Below-ground cages Wooden-sided cages Control (no cage)
(1) Incubation duration (days) 97.0, n= 1 (2010);
89.3 ± 4.5, n= 4 (2011)
–(2010);
83.5 ± 3.5, n= 2 (2011)
–(2010);
94.0 ± 5.8, n= 4 (2011)
94.2 ± 3.4, n= 6 (2010);
97.3 ± 3.1, n= 3 (2011)
(2) Hatching success (%) 69.3 ± 8.0, n= 24 79.1 ± 6.7, n= 25 76.4 ± 4.4, n= 12 59.7 ± 8.8, n=20
(3) Proportion of deformed
hatchlings per clutch
0.23 ± 0.1, n= 6 (2010);
0.18 ± 0.06, n= 10 (2011)
0.41 ± 0.11, n= 10 (2010);
0.30 ± 0.08, n= 10 (2011)
–(2010);
0.36 ± 0.06, n= 12 (2011)
0.37 ± 0.12, n= 8 (2010);
0.33 ± 0.05, n= 9 (2011)
(4) Number of deformities
per turtle per clutch
0.30 ± 0.12, n= 6 (2010);
0.38 ± 0.14, n= 10 (2011)
1.23 ± 0.41, n= 10 (2010);
0.55 ± 0.2, n= 10 (2011)
–(2010);
0.63 ± 0.1, n= 12 (2011)
0.73 ± 0.27, n= 8 (2010);
0.59 ± 0.12, n= 9 (2011)
(5) Number of hatchlings
that failed to right
3, n=91 5, n= 115 3, n=63 9,n=77
(6) LP (s) 73.9 ± 11.6, n= 86 126.0± 13.9, n= 114 106.0 ± 17.6, n= 62 128.6 ± 17.1, n=70
(7) RP (s) 11.6 ± 4.1, n= 86 23.1 ± 8.0, n= 114 11.0 ± 5.1, n= 62 12.4 ± 4.0, n=70
Table 6. Summary of Chelydra serpentina clutch and hatchling data
Data are means s.e. For the first four variables (1–4), samples size (n) represents the number of nests, and for the last three variables (5–7), nrepresents the number
of hatchlings. If data were analysed between years, means are shown separated by commas, and in some instances, year data were pooled. LP, latency period; RP,
righting period
Clutch and hatchling variable Nest-cage treatment
Above-ground cages Below-ground cages Wooden-sided cages Control (no cage)
(1) Incubation duration (days) 93 ± 2.2, n= 10 (2010);
88.1 ± 3.0, n= 10 (2011)
92.7 ± 1.8, n= 9 (2010);
89.8 ± 1.9, n= 12 (2011)
–(2010);
89.4 ± 2.0, n= 8 (2011)
93.4 ± 2.7, n= 7 (2010);
89.8 ± 2.7, n= 11 (2011)
(2) Hatching success (%) 82.2 ± 6.9, n= 23 85.2 ± 4.2, n= 21 73.2 ± 12.0, n= 10 73.0 ± 7.0, n=20
(3) Proportion of deformed
hatchlings per clutch
0.27 ± 0.06, n= 10 (2010);
0.24 ± 0.07, n= 10 (2011)
0.36 ± 0.06, n= 11 (2010);
0.28 ± 0.06, n= 12 (2011)
–(2010);
0.25 ± 0.07, n= 8 (2011)
0.28 ± 0.08, n= 8 (2010);
0.14 ± 0.04, n= 11 (2011)
(4) Number of deformities per
turtle per clutch
0.47 ± 0.12, n= 10 (2010);
0.41 ± 0.14, n= 10 (2011)
0.72 ± 0.2, n= 11 (2010);
0.53 ± 0.2, n= 12 (2011)
–(2010);
0.41 ± 0.1, n= 9 (2011)
0.54 ± 0.2, n= 8 (2010);
0.19 ± 0.06, n=11 (2011)
(5) Number of hatchlings
that failed to right
53, n= 599 42, n= 643 21, n= 271 19, n= 481
(6) LP (s) 75.2 ± 6.0, n= 546 67.1 ± 5.1, n= 634 108.3 ± 9.6, n= 250 93.7 ± 7.1, n= 429
(7) RP (s) 3.9 ± 0.9, n= 546 6.7 ± 1.9, n= 634 5.5 ± 1.8, n= 250 11.6 ± 2.8, n= 429
Table 7. Summary of the cost analysis for each nest cage design
The costs shown are per single nest cage. Salary cost was CAN$10.25/h, the minimum wage in Ontario, Canada
Nest-cage type Material
cost ($)
Construction
time (min)
Installation
time (min)
Total
time (min)
Salary
cost (CAN$)
Total
cost (CAN$)
Wooden-sided cages 2.20 15 (n= 25) 6 (n= 7) 21 3.60 5.80
Below-ground cages 4.90 82 (n=5) 13 (n= 14) 95 16.20 21.10
Above-ground cages 9.10 100 (n= 15) 10 (n= 7) 110 18.80 27.90
HWildlife Research J. L. Riley and J. D. Litzgus
Table 7). The total cost, including materials and salary, was
lowest for wooden-sided cages (Table 7).
Discussion
Nest environment
Most environmental characteristics did not differ among nest-
cage types. Around painted turtle nests with wooden-sided cages,
the percentage of woody plants was greater than that in all other
treatments. Installing wooden-sided cages did not involve
digging through plant roots, whereas installation of the other
cages involved digging 20 cm below ground through plant roots.
Thus, differences in cage-installation requirements may alter the
vegetation around the nest from what was maternally selected.
Most thermal-environment characteristics did not differ
among treatments, which did not support our prediction that
nest-cage materials would shade and reduce the temperature
within the nest. Nest temperature, temperature during each
third of embryo development, and heat units did not differ
among treatments. Daily temperature variance in snapping
turtle nests was lower in the wooden-sided than below-ground
cage treatment, but not different among any other treatments
for snapping or painted turtles. Wooden-sided cages appear
to reduce temperature fluctuations in snapping turtle nests.
Overall, the thermal environment of the nest was not altered
greatly from natural conditions by any of the nest-cage types.
These findings indicated that nest cages preserve most of the
thermal characteristics that females select to maximise hatching
success, and turtle researchers who use above- and below-ground
nest cages in their studies are recording temperature data
reflective of natural conditions.
None of the nest-cage types tested in our study altered
temperature from natural conditions during the TSD thermo-
sensitive period. During the thermo-sensitive period, painted
turtle embryos across all treatments were incubated at a mean
of 25C, with a daily temperature variance of 20C. According
to the variable degree model of TSD in painted turtles, if
development in the thermo-sensitive period occurs between
22C and 28C, then that clutch will be entirely male (Bull and
Vogt 1981; Neuwald and Valenzuela 2011). However, both
male and female painted turtles occur at our study site, which
may be attributable to temperature fluctuations during the thermo-
sensitive period having a feminising effect on the embryos (Les
et al.2007; Paitz et al.2010; Neuwald and Valenzuela 2011), or
as a result of prior higher annual temperatures. Snapping turtles
across all treatments were incubated at a mean of 26C, with a
daily temperature variance of 5C; this mean temperature is
known to result in development of males (Wilhoft et al.1983),
but does not account for an effect of thermal variance, which has
also been found to affect sex ratio in C. serpentina (Freedberg
et al.2011). In recent years, conservation concerns have grown
over road mortality of females that results in male-biased
populations, and global warming which also may skew sex
ratios (Mrosovsky and Provancha 1989; Steen and Gibbs
2004; Hawkes et al.2007). As cages were not found to alter
nest temperature, wildlife managers could not use nest cages to
promote equal sex ratios in turtle populations where sex ratio is
skewed. More importantly, nest caging does not appear to alter
nest temperatures in a way that will affect TSD in turtles.
Clutch and hatchling characteristics
Incubation duration did not differ among treatments, which was
expected because incubation duration is inversely related to
incubation temperature and there were no differences in
temperature among cage treatments. In central Ontario, near
the northern range limits of turtles, this is critical knowledge
as conservation strategies must take into account a short active
season. Nest cages did not extend incubation into colder months
that could prevent development, and/or force over-wintering
within the nest (Bobyn and Brooks 1994). Also, nest cages did
not alter hatching success from natural levels. Thus, nest cages
are a conservation tool that maintains natural levels of hatching
success within the natural emergence period, while in turn
increasing the amount of nest success by protecting nests from
predators.
Some proxies of hatchling fitness did not differ among
treatments. Deformity rates and locomotor performance (LP
and RP) did not differ among treatments, which is not
surprising because incubation temperature affects both of these
proxies (McKnight and Gutzke 1993; Díaz-Paniagua et al.1997;
Hewavisenthi and Parmenter 2001; Steyermark and Spotila
2001) and we found no differences in temperature among cage
treatments. Hatchling body condition, another proxy for fitness,
varied among treatments and the effects of cages on body
condition were not consistent between species. For painted
turtles, wooden-sided cages, and for snapping turtles, below-
ground cages had positive effects on body condition. Above-
ground cages negatively affected body condition of snapping
turtles. Species-specific differences may be due to differences in
nest environment. Nest-site preferences differ between painted
and snapping turtles (Schwarzkopf and Brooks 1987; Weisrock
and Janzen 1999; Kolbe and Janzen 2002; Hughes and Brooks
2006). We found that the amount of woody plants around nests
was different among treatments in painted turtles but not
snapping turtles. Also, nest-temperature variance was much
greater in the nests of painted turtles than in the nests of
snapping turtles, which may relate to the fact that snapping
turtles lay nests about two times deeper than do painted turtles
(Ernst and Lovich 2009); the greater depth buffers the nest from
temperature fluctuations (Spotila 2011). The differences found
between species highlighted the importance of a multi-species
approach to the evaluation of conservation techniques. Additional
species-specific evaluation of this conservation tool is necessary
for species with nest characteristics that differ greatly from the
species studied here (e.g. sea turtles; Spotila 2011).
Differences in body condition among treatments did not
appear to be driven by the hypothesised mechanism (shading
by cage material) because incubation temperature did not differ
among treatments. In contrast to our predictions, hatchlings
incubated in wooden-sided and above-ground cages (the cages
with the potential for shading) did not have the poorest body
conditions. So, what is the mechanism behind the differences
found? Temperature variance differed significantly among
treatments in snapping turtles. Nests with below-ground cages
had the most variable temperatures of all the treatments (Table 4)
and produced hatchlings that were heavier across all carapace
lengths. Painted turtles incubated in wooden-sided cages were
heavier than hatchlings at the same carapace length in other
Effects of predator-exclusion cages on turtle nests Wildlife Research I
treatments, and even though a difference was not found among
treatments, nest temperature was less variable than in the other
treatments (Table 3). Perhaps temperature variation, and in turn
hatchling body condition, are affected by nest-cage type, and
the effect differs between species. Shallow painted turtle nests
experience more temperature variance, so reducing the variance
by using wooden-sided cages may be beneficial, whereas in
snapping turtles, increasing the variance is not harmful (and
may even be beneficial) because they generally experience low
variance in their deep nests. It would appear that a moderate
amount of temperature variance (~10C) may improve body
condition, and this is achieved by lowering variance in painted
turtle nests and increasing variance in snapping turtle nests.
Furthermore, temperature variation influences the development
of turtles and has been found to affect body size, locomotor
performance and growth in various species (Doody 1999;
Ashmore and Janzen 2003; Du and Ji 2003; Booth 2006; Les
et al.2007; J. L. Riley, S. Freedberg and J. D. Litzgus 2013,
unpubl. data). Alternatively, other measures of nest environment
that were not measured in our study may have been affected by
nest-cage type, and may have driven the differences in hatchling
body condition among cage types. Overall, more research is
needed to uncover the mechanism driving the differences in
hatchling body condition among treatments.
Predators and nest cages
Predator interactions with nest cages and successful depredation
events did not differ among nest-cage types. This indicates that
predators are not attracted to one nest-cage type over another, and
that all nest-caging types are equivalent in protecting turtle nests.
Similarly, Burke et al.(2005) and Strickland et al.(2010) found
that marking nests did not increase raccoon depredation rates.
Additionally, Kurz et al.(2011) found that an enlarged version of
the above-ground cage in our study did not attract foxes over
other, less conspicuous, cage types. In contrast, Mroziak et al.
(2000) found that nest caging may cue raccoons to the presence
of a nest and attract depredation attempts. In an 8-year study,
Rollinson and Brooks (2007) found that Corvus sp. used nest
markers as visual cues of nests. Within a short-term study period
(2 years), nest cages or nest flags are not likely to be a ‘learned’cue
for nest predators; however, over the long term, certain predator
species may learn to associate nest markers with a food source.
In our study, above-ground and wooden-sided cages both had
instances where after repeated predator interactions, the nest was
successfully depredated. Cages, such as these, that extend above
ground level may attract multiple predation interactions, which
increase both the probability of nest predation, and opportunities
to learn that nest cages cue a food source. It is also important to
note that our study was conducted in an area where predation
pressures were relatively low. In areas where subsidised predators
are abundant, or where burrowing predators (like snakes and
rodents) are present, cages that extend underground around the
nest cavity may be desirable (Rodríguez-Robles 1998; Converse
et al.2002; Plummer 2010).
Cost analysis of nest-cage designs
Often, the biggest constraint for conservation actions is funding.
Our cost analysis showed that wooden-sided cages were the most
cost-effective design. Wooden-sided cages are also simple for
volunteers to construct (Mersey Tobeatic Research Institute and
Parks Canada 2009). However, there are other factors to consider.
For instance, nest caging that extends above the ground
(potentially paired with an educational sign) could be used to
increase public awareness of the threats facing turtle populations
(Newbury et al.2002). At study sites in Algonquin Park, many
park visitors took interest in our nest cages. Signs were posted
around the study sites, which often prompted the public to engage
in discussions regarding actions an individual could take to
restore turtle populations. But, if other concerns are driving
decisions about nest caging, for example maximising crypsis
of nest cages in areas where disturbance from the public is
prevalent (Bolton et al.2008), or if threats of poaching exist,
then other nest-caging types, such as below-ground cages, should
be employed. The highest priority in a management program
should be to maximise nest success and hatchling fitness, but it
is understandable that wildlife managers need to also consider
logistical, funding and goal-based concerns when choosing a
nest-cage type for conservation programs.
Conclusions
Overall, nest cages did not substantially alter the nest environment
from natural conditions. Above-ground cages negatively affected
body condition in one species, but the other cage types did not
negatively affect hatchling fitness, indicating that they are
effective conservation tools that do not present secondary
deleterious effects on potential recruitment. In conservation of
long-lived species, such as turtles, it is important to pay attention
to indicators of survival in early life stages because it is difficult
to see the population-level outcomes of recovery actions for
decades, which delays evaluation and adaptive management
(Spencer and Janzen 2010). The effects of nest-cage types on
hatchling body condition differed between species, perhaps due
to differences in nest depth and thermal regimes. Selection of a
nest-cage type for conservation strategies should be based on
maximising nest success, hatchling fitness, and on logistical
concerns (e.g. ease and efficiency of construction, installation
and material costs). Our evaluation of nest caging provides
essential knowledge to researchers, wildlife managers, and
conservationists for use globally in at-risk turtle-management
strategies and research.
Acknowledgements
Financial support was provided by Natural Sciences and Engineering
Research Council (NSERC; CGS-M scholarship to JLR and Discovery
Grant to JDL), Canadian Wildlife Federation, Ontario Ministry of Natural
Resources (OMNR), Toronto Zoo, and Laurentian University. In-kind
contributions were provided by Algonquin Provincial Park (OMNR) and
University of Guelph. The following people assisted with fieldwork:
M. Keevil, P. Moldowan, K. Hall, H. McCurdy-Adams and L. Monck-
Whipp. All work was carried out under an approved Laurentian University
Animal Care Committee protocol (AUP # 2008-12-02) and was authorised by
permits from OMNR.
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