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The importance of passive integrated transponder (PIT) tags
in population monitoring
Kelle Holmes
University of Exeter, Penryn Campus 630030391
Keywords: Chelonia mydas, Caretta caretta, tag-loss, PIT, monitoring Word count: abstract: 137, main: 4527 59 references, 3 figures, 2 tables
Supervisor: Annette Broderick
1
Abstract
In the study of life history traits, it is important to be able to re-identify individuals. Long-term
individual-based monitoring of green and loggerhead turtles at Alagadi, northern Cyprus is
providing fundamental and applied insights into marine turtle life histories. For both species,
tag loss probability for plastic flipper, titanium flipper, and passive integrated transponder
(PIT) tags was calculated. For both green and loggerhead turtles, tag loss probabilities were
greater having accounted for the use of PIT tags to help identify a female. This would have
resulted in over-estimation of green turtle recruitment by 44% and loggerhead recruitment
by 25%. The present study highlights the importance of PIT tag use in long term population
monitoring to reduce population estimate bias resulting from tag loss. Proficiency of tagging
procedures, double tagging and potential tag loss causes are also discussed.
Introduction
A basic tool for understanding and conserving wildlife populations is population modelling
(Nicholes and Williams, 2006). Credible development of population models needs accurate
and reliable reproductive and survival estimates. Population assessments can be made
difficult when individuals may have large ranges and be difficult to sample and re-identify
(Baily, 1951, Sedinger et al, 2008). These problems are particularly profound for marine
animals as they can remain submerged for long periods of time and move across thousands
of kilometres (Rasmussen et al. 2007). Estimating populations can be made easier when the
study species exhibits predictable migrations or nesting aggregations (for example harbour
seals (Thompson et al., 2005), white sharks (Jorgensen et al. 2009) and marine turtles
(Broderick et al., 1996)).
Monitoring programmes heavily rely on the ability to identify individuals over-time
(Balazs, 1999). The re-identification of individual animals can be achieved in a number of ways:
natural markings (Katona and Whitehead, 1981 and Kelly, 2001), branding (McMahon et al.,
2006), bands (Dugger et al., 2006), identification microchips (Gibbons and Andres, 2004;
Harper and Batzli, 1996 and Buhlmann and Tuberville, 1998), rings (Lakhani, 1987 and
Kenward et al., 2000), ear and flipper tags (Morley, 2002). Recognising individual markings is
often the most challenging way to re-identify an individual (Stevick et al., 2001). Therefore,
many population monitoring programs mark individuals using tags. Animals are often marked
with two tags to maximise the chance that upon recapture the individual will have at least one
2
tag still attached (rather than presumed dead and lost to the study). The inability to recognise
a tag either through illegibility, damage or physical loss (hereafter termed tag loss) can
become a major confounding variable for re-identification experiments (Arnason and Mills,
1981). Population estimates derived from tag returns can often be inaccurate, owing to tag
loss errors (Arnason and Mills, 1981 and Stobo and Horne, 1994). Failure to consider tag loss
in any monitoring program will lead to over estimations of population abundance,
underestimations of survival and subsequent bias in data and further analyses. The
development of photo identification techniques for re-identification are becoming more
common amongst marine turtle research groups (Reisser et al., 2008, Schofield et al., 2008).
However, the most established method for marine turtle re-identification is through the use
of metal or plastic flipper tagging techniques alongside Passive Integrated Transponder
(hereafter PIT) tags. During a study on green turtles at Ascension Island, Mortimer and Carr
(1987) reported 78% tag loss and upper retention estimates of just six years. Previous studies
have attributed marine turtle tag loss to a variety of reasons. These include: tag position, tag
application, tag type, tag material, species of turtle and subsequent lifestyle differences
including the environment that the turtle is in (Reisser et al., 2008; Limpus, 1992; Balazs,
1982).
Loggerhead turtles (Caretta caretta) and Green turtles (Chelonia mydas) in the
Mediterranean migrate from their North African feeding grounds to on the beaches of Cyprus,
Turkey and Greece. A turtle that is new to the population is termed a neophyte. Female green
and loggerhead turtles do not breed every single year. The interesting period (termed
remigration) is variable due to fluctuating environmental factors and individual body condition
(Solow et al., 2002; Broderick et al., 2003). Females will lay multiple clutches inter-annually
(Stokes et al 2014). Turtle populations are vulnerable to many anthropogenic disturbances
(Snape et al., 2016; Nada and Casale, 2011; Godley et al., 1998) which have subsequently led
to their decline and both species are currently of conservation concern (Casale and Tucker,
2015 and Seminoff, 2004).In order to quantify these threats, we need to understand more
about their life history traits, of which there is still a lot unknown. At Alagadi, northern Cyprus,
a saturated tagging programme is used to monitor green and loggerhead females during the
nesting season. This is part of an on-going effort to understand how variations in their life
history traits impact on population dynamics, survival, growth and behavioural strategies. The
findings are then used to put in place effective management interventions for conservation.
3
After twenty years of monitoring, long-term data sets are being generated. However, if valid,
reliable studies based on tag return data are to proceed, then the issue of tag loss needs to
be addressed.
The first objective of this study was to estimate the tag loss probabilities for different
tag types using the method as described by Limpus (1992). The second objective was to
investigate the ramifications of tag loss assumptions and to determine how lack of detection
could have affected tag loss estimates. The effect of double tagging and potential causes of
tag loss are also discussed.
Methods
The study was conducted on Alagadi beach, in Northern Cyprus where both green and
loggerhead turtles are found nesting in considerable numbers (Broderick and Godley, 1996).
Throughout the nesting season the 2km beach is closed to the public between 2000 and 0800
hours (+3hGMT) in order to minimise anthropogenic disturbance.
Tagging and Recapture of Turtles
Data were collected throughout the nesting seasons of 1992-2015. Patrols ran along the beach
from 21:00 to 06:00 hours (local time) each night between late May and mid-August with
monitoring ceasing after five days of no nesting activity (Broderick and Godley, 1996). Once a
female was observed laying, she was examined for existing tags. If the female had no tag, lost
one tag or a tag had become unreadable, then a new tag was attached. Females were tagged
whilst in the covering phase, immediately after completion of oviposition. Both green and
loggerhead females were tagged on the trailing edge of the fore-flippers in the thin skin
between the proximal second and third scales. PIT tags were injected under the skin in the
shoulder. Where possible females were given flipper tags on both fore-flippers and
occasionally in both shoulders to avoid the loss of the turtle ID (Björnsson et al., 2011). Flipper
tags used were self-piercing with self-locking ‘through the hole’ mechanism. They were
attached using the respective specific tag applicators as supplied by the tag manufacturer. No
local anaesthetic was used as the piercing procedure is instantaneous. From 1992 to 1999
green and loggerhead females were tagged with plastic flipper tags (Dalton Jumbotags® used
1992-1994, Dalton Supertag® used 1994-1999; Dalton Tags, UK). From 1999-2015 titanium
Stockbrands® (Australia) flipper tags were used - with the exception of 2014 where Inconel
4
681/C tags where used (National Band & Tag Company, Kentucky, USA). PIT tags have been
used in addition to double-flipper tags since 1997. This ‘triple tagging’ method ensures
greater chance of identification from recaptures. Although in some cases females have
reacted to tagging by withdrawing their limbs or inhaling sharply, Broderick and Godley (1999)
have shown there to be no significant effects of tagging on the speed of descent, duration of
nesting behaviours or hatching success of clutches.
Estimation of Tag Loss
Tag loss was estimated and analysed separately for both green and loggerhead females. Tag
loss was estimated with respect to turtle species, tag age and tag type. Each tag was
considered independently and, for each tag, years since application (to the nearest whole
year), and presence or absence was recorded. Tag loss probability was calculated as per the
following Limpus (1992) equation: 𝑃𝑖 = 𝑏𝑖/(𝑎𝑖 + 𝑏𝑖) where, 𝑖 = number of years since tag
was applied (ie. tag age); 𝑎𝑖 = number of tags still attached to the recaptured turtle in year 𝑖
with a readable number; 𝑏𝑖 = number of tags lost/unreadable from recaptured turtles in year
𝑖; 𝑃𝑖 = the probability of a tag being lost or unreadable after 𝑖 years.
Results
For both species there were insufficient tag recoveries of Monel tags used in 2014 due to
remigration intervals and so these were excluded from all analysis. Estimates of tag loss
probabilities from recaptures up to an including 2015 for green and loggerhead are
summarised in Table 1.
Green Turtles (Chelonia mydas)
A total of 302 individually identifiable nesting green female turtles have been tagged at
Alagadi since 1992 and were included in this study. 38.74% (n=43) of neophytes nesting
between 1997 and 2010 did not re-migrate to this site in subsequent breeding seasons (2011-
2015 are not included here as these turtles may still return). Over eighteen years, there were
failed readings of the PIT tags of 31.85% (n=50) green turtles, of which 20.0% (n=10)
subsequently received an additional PIT tag. Of 307 titanium tags included in this study, 65%
(n=200) were lost before the turtle made its next migration to Alagadi. Of these tags, 93%
(n=186) were lost within six years, and 54% (n=107) were lost within three years.
5
Table 1. Frequency distribution of tag loss for tags applied to Chelonia mydas and Caretta caretta in Alagadi, northern Cyprus, 1992-2015.
𝑎𝑖, number of tags still attached to recaptured turtle in year 𝑖 with a readable number; 𝑏𝑖, number of tags lost/unreadable from recaptured turtles in year 𝑖; CL, confidence limits
Chelonia mydas Caretta caretta
Tag Type Tag age (year 𝑖)
Tag Count Probability of loss ± 95% CL
Tag Count Probability of loss ± 95% CL 𝒂𝒊 𝒃𝒊 total 𝒂𝒊 𝒃𝒊 total
PIT 1 2 0 2 0∙000 ± 0∙000 12 1 13 0∙077 ± 0∙000 2 42 4 46 0∙087 ± 0∙058 41 5 46 0∙108 ± 0∙000 3 66 8 74 0∙108 ± 0∙051 36 4 40 0∙100 ± 0∙000 4 86 6 92 0∙065 ± 0∙036 23 5 28 0∙179 ± 0∙000 5 27 2 29 0∙068 ± 0∙065 29 4 33 0∙121 ± 0∙000 6 44 1 45 0∙022 ± 0∙031 17 1 18 0∙056 ± 0∙000 7 23 0 23 0∙000 ± 0∙000 10 0 10 0∙000 ± 0∙000 8 21 1 22 0∙045 ± 0∙062 6 0 6 0∙000 ± 0∙000 9 21 0 21 0∙000 ± 0∙000 13 0 13 0∙000 ± 0∙000 10 12 0 12 0∙000 ± 0∙000 5 0 5 0∙000 ± 0∙000 11 7 0 7 0∙000 ± 0∙000 4 0 4 0∙000 ± 0∙000 12 20 0 20 0∙000 ± 0∙000 9 0 9 0∙000 ± 0∙000 13 14 0 14 0∙000 ± 0∙000 1 0 1 0∙000 ± 0∙000 14 7 0 7 0∙000 ± 0∙000 2 0 2 0∙000 ± 0∙000 15 9 0 9 0∙000 ± 0∙000 16 16 0 16 0∙000 ± 0∙000 1 0 1 0∙000 ± 0∙000 17 5 1 5 0∙167 ± 0∙213 5 0 5 0∙000 ± 0∙000 18 2 0 2 0∙000 ± 0∙000
Plastic 1 5 1 6 0∙167 ± 0∙213 2 25 4 29 0∙138 ± 0∙008 21 7 28 0∙250 ± 0∙000 3 27 15 42 0∙357 ± 0∙011 13 3 16 0∙188 ± 0∙000 4 9 10 19 0∙526 ± 0∙026 11 4 15 0∙267 ± 0∙000 5 18 13 31 0∙419 ± 0∙015 10 8 18 0∙444 ± 0∙000 6 7 10 17 0∙588 ± 0∙028 6 3 9 0∙333 ± 0∙000 7 1 15 16 0∙938 ± 0∙007 2 1 3 0∙333 ± 0∙000 8 8 6 14 1∙400 ± 0∙034 0 2 2 1∙000 ± 0∙000 9 0 3 3 1∙000 ± 0∙000 0 5 5 1∙000 ± 0∙000 10 3 2 5 1∙000 ± 0∙094 2 3 5 0∙600 ± 0∙000 11 0 1 1 1∙000 ± 0∙000 12 0 6 6 1∙000 ± 0∙000 1 0 1 0∙000 ± 0∙000 13 0 3 3 1∙000 ± 0∙000 0 1 1 1∙000 ± 0∙000 14 0 2 2 1∙000 ± 0∙000 15 16 17 0 1 1 1∙000 ± 0∙000 18 0 1 1 1∙000 ± 0∙000
6
Table 1. continued
Titanium 1 1 2 3 0∙667 ± 0∙145 5 1 6 0∙167 ± 0∙213 2 19 39 58 0∙672 ± 0∙007 21 7 28 0∙250 ± 0∙115 3 44 63 107 0∙589 ± 0∙004 13 3 16 0∙188 ± 0∙137 4 31 81 112 0∙723 ± 0∙004 11 4 15 0∙267 ± 0∙160 5 11 12 23 0∙522 ± 0∙021 10 8 18 0∙444 ± 0∙164 6 15 8 23 0∙348 ± 0∙019 6 3 9 0∙333 ± 0∙220 7 7 5 12 0∙417 ± 0∙040 2 1 3 0∙333 ± 0∙381 8 6 10 16 0∙625 ± 0∙029 0 2 2 1∙000 ± 0∙000 9 5 9 14 0∙643 ± 0∙032 0 5 5 1∙000 ± 0∙000 10 3 2 5 0∙400 ± 0∙094 2 3 5 0∙600 ± 0∙307 11 12 2 4 6 0∙667 ± 0∙073 1 0 1 0∙000 ± 0∙000 13 1 0 1 0∙000 ± 0∙000 1 0 1 0∙000 ± 0∙000 14 1 1 2 0∙500 ± 0∙245 1 1 2 0∙500 ± 0∙000
Without the use of PIT tags Plastic 1 5 1 6 0∙167 ± 0∙213 2 25 3 28 0∙107 ± 0∙082 20 4 24 0∙167 ± 0∙107 3 27 6 33 0∙182 ± 0∙094 13 2 15 0∙133 ± 0∙123 4 9 2 11 0∙182 ± 0∙163 11 4 15 0∙267 ± 0∙160 5 18 7 25 0∙280 ± 0∙126 10 6 16 0∙375 ± 0∙170 6 6 4 10 0∙400 ± 0∙617 6 1 7 0∙143 ± 0∙185 7 1 8 9 0∙889 ± 0∙147 2 1 3 0∙333 ± 0∙381 8 8 1 9 0∙111 ± 0∙147 0 1 1 1∙000 ± 0∙000 9 0 2 2 1∙000 ± 0∙000 0 3 3 1∙000 ± 0∙000 10 3 0 3 0∙000 ± 0∙000 2 3 5 0∙600 ± 0∙307 11 12 0 4 4 1∙000 ± 0∙000 1 0 1 0∙000 ± 0∙000 13 0 1 1 1∙000 ± 0∙000 Titanium 1 1 0 1 0∙000 ± 0∙000 9 1 10 0∙100 ± 0∙133 2 16 12 28 0∙429 ± 0∙131 26 9 35 0∙011 ± 0∙103 3 39 16 55 0∙291 ± 0∙086 23 10 33 0∙013 ± 0∙112 4 29 20 49 0∙408 ± 0∙098 16 4 20 0∙016 ± 0∙250 5 11 3 14 0∙214 ± 0∙154 7 5 12 0∙040 ± 0∙199 6 14 6 20 0∙300 ± 0∙143 3 2 5 0∙094 ± 0∙307 7 7 1 8 0∙125 ± 0∙164 6 1 7 0∙034 ± 0∙185 8 5 0 5 0∙000 ± 0∙000 3 1 4 0∙092 ± 0∙303 9 5 2 7 0∙286 ± 0∙240 2 0 2 0∙000 ± 0∙000 10 3 1 4 0∙250 ± 0∙303 1 0 1 0∙000 ± 0∙000 11 2 0 2 0∙000 ± 0∙000 12 2 2 4 0∙500 ± 0∙350 1 0 1 0∙000 ± 0∙000 13 1 0 1 0∙000 ± 0∙000 14 1 0 1 0∙000 ± 0∙000 1 1 2 0∙245 ± 0∙495
7
PIT tag loss was considerably less than that of both flipper tag types (mean annual
probability of loss = 0.0313, and for combined flipper tags = 0.609). The greatest flipper tag
loss was associated with plastic flipper tags (mean annual probability of loss = 0.720, titanium
tag mean annual probability of loss = 0.521). All flipper tag loss probability estimates for green
were greater having accounted for the use of PIT tags to help identify a female without flipper
tags (Figure 1). Without accounting for the use of PIT tags to help identify a female, mean
annual probability of plastic tag loss was 0.415, for titanium tags 0.216 and for both flipper
tag types combined 0.244.
(a) PIT
(b) Flipper
(c) Plastic
(d) Titanium
Figure 1: Probability of tag loss for Chelonia mydas in Alagadi, Northern Cyprus. a) PIT tags b) Flipper tags (plastic and titanium combined) c) Plastic tags d) Titanium tags. Solid circles represent tag loss estimates having accounted for the use of PIT tags to help identify a female. Open circles represent tag loss estimates without accounting for the use of PIT tags
8
The results for the number of returning green turtles that lost both flipper tags and were
identified by PIT tag only are summarised in Table 2 and Figure 2a (1997-2008 are not included
here to ensure that all potential returning turtles would had been given a PIT tag). On average
44.16% of green turtles were identified by PIT tag alone as a result of having lost both of their
flipper tags. Therefore, without the use of PIT tags, flipper tag loss would result in a 44.16%
over-estimation of green turtle neophytes.
Loggerhead Turtles (Caretta caretta)
A total of 342 individually identifiable nesting female loggerhead have been tagged at Alagadi
since 1992 and were included in this study. 72.69% (n=157) of neophytes nesting between
1997 and 2010 did not re-migrate to this site in subsequent breeding seasons (2011-2015 are
not included here as these neophytes may still return). Over eighteen years, there were failed
readings of the PIT tags of 30.56% (n=44) loggerhead turtles, 31.82% (n=14) of which
subsequently received an additional PIT tag. Of 134 titanium tags included in this study, 50%
(n=68) were lost before the turtle made its next migration to Alagadi. Of these tags, 99%
(n=67) were lost within six years, and 74% (n=50) were lost within three years.
PIT tag loss was considerably less than that of both flipper tag types (mean annual
probability of loss = 0.040 and for combined flipper tags = 0.433). The greatest flipper tag loss
was associated with plastic flipper tags (mean annual probability of loss = 0.466, titanium tag
Table 2. Number of returning Chelonia mydas and Caretta caretta that have lost both flipper tags and were identified by PIT tag only
x, number of turtles identified by PIT tag only (i.e. had no flipper tags); r, total number of turtles identified as ‘returns’ by flipper tags and/or PIT tags; n, number of turtles
identified as neophytes due to the absence of both PIT and flipper tags; %, percent of returning turtles hat would have been incorrectly identified as neophytes if not for the
use of PIT tags.
Chelonia mydas Caretta caretta Year x r n total % x r n total %
2009 10 18 22 41 55∙56 2 11 21 34 15∙38 2010 1 12 15 27 08∙33 0 3 16 19 00∙00 2011 7 20 32 54 35∙00 4 5 13 22 44∙44 2012 10 14 9 23 71∙43 0 5 14 20 00∙00 2013 7 26 61 86 26∙92 2 6 35 41 25∙00 2014 19 28 31 59 67∙86 1 4 28 35 20∙00 2015 11 25 36 61 44∙00 4 2 20 26 66∙67
Average % (mean) 44∙16 24∙50
9
mean annual probability of loss = 0.331). All flipper tag loss probability estimates for
loggerheads were greater having accounted for the use of PIT tags to help identify a female
without flipper tags (Figure 3). Without accounting for the use of PIT tags to help identify a
female, mean annual probability of plastic tag loss was 0.432, for titanium tags 0.198 and for
both flipper tag types combined 0.333.
The results for the number of returning loggerhead turtles that lost both flipper tags and
were identified by PIT tag only are summarised in Table 2 and Figure 2b (1997-2008 are not
included here to ensure that all potential returning turtles had been given a PIT tag). On
average 24.50% of loggerhead turtles were identified by PIT tag alone as a result of having lost
both of their flipper tags. Therefore, without the use of PIT tags, flipper tag loss would result
in a 24.50% over-estimation of loggerhead turtle neophytes.
For plastic tags, species did not significantly contribute to tag loss (R2=0.09, P>0.05). For
titanium tags species contributed significantly to tag loss (R2=0.28, P<0.01) with loggerhead
having lower tag loss estimates than green. Species contributed significantly to PIT tag loss
(R2=0.22, P<0.05) with green having much lower tag loss estimates than loggerhead.
(a) Chelonia mydas (b) Caretta caretta
Figure 2: The number of returning a) green and b) loggerhead turtles identified using PIT tags only having lost both flipper tags. turtles identified as a neophyte due to the absence of flipper tags a PIT tags, turtles identified using PIT tags and flipper tags, turtles identified using PIT tag only
0
10
20
30
40
50
60
70
80
90
2009 2010 2011 2012 2013 2014 2015
Nu
mb
er o
f Tu
rtle
s
Year
0
5
10
15
20
25
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2009 2010 2011 2012 2013 2014 2015
Nu
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10
(a) PIT
(b) Flipper
(c) Plastic
(d) Titanium
Figure 3: Probability of tag loss for Caretta caretta in Alagadi, Northern Cyprus. a) PIT tags b) Flipper tags (plastic and titanium combined) c) Plastic tags d) Titanium tags. Solid circles represent tag loss estimates having accounted for the use of PIT tags to help identify a female. Open circles represent tag loss estimates without accounting for the use of PIT tags
11
Discussion
Variation between Tag Types
Results from the present study are evidence of strong differences in the effect of tag type on
the probability of tag loss (Figure 1 and Figure 3).
For both species, the greatest tag loss was associated with plastic flipper tags. Plastic
tags do not suffer from corrosion and, due to their locking mechanisms do not often fall out.
The most common reason for plastic flipper tag loss is that after five to six years, the tags are
deemed illegible. This means the turtle is no longer identifiable by this tag and would need
to be removed and replaced. For green turtles, the average duration of an attached, legible
plastic tag was six years and for loggerhead turtles five years. As remigration intervals are up
to six years for both green and loggerhead turtles (Stokes et al., 2014), it is unlikely that a
female would be recaptured on its next migration with both tags still legible. This will
drastically reduce the chance of successful re-identification in a long-term study. For
population trends to be detected, a minimum of three data points are required. Parmenter
(2003) reported plastic tag failures in flatback turtles (Natator depressus) of up to 80% within
the first three years of application. Due to the remigration intervals, a marine turtle tagging
programme would need to run for ten to fifteen years before it is possible to detect trends in
abundance which means plastic tag use would be inappropriate. Plastic tags have the
advantage of colour coding. By using a different colour for each tagging site, it is possible to
identify the origin on the individual without it having to be captured. This is particularly useful
when projects are working with fishermen to determine by-catch risk, or to gain re-sightings
of the tags by the public or other projects that do not have a PIT tag scanner. However, it has
been documented that plastic tags may increase the probability of a turtle becoming
entangled in fishing nets (Nichols et al., 1998). This has been supported by interviews with
local fishermen and an aquarium study that showed only tagged individuals were unable to
escape from entanglement in a net (Nichols et al., 1998). In sea turtle research, the use of
plastic tags should be limited to short-term studies on resident marine turtle populations and
are not necessarily fit for use in long-term tag return studies.
Titanium flipper tags had lower tag loss estimates than plastic flipper tags (Table 1).
Difference in species contributed to the variation in titanium tag loss rates between
loggerhead and green. For green, there was a significant decrease in titanium tag loss with
12
increasing tag age. This reflects results by Rivalan et al. (2005) which showed metal tag loss
probabilities for leatherbacks were initially high for the first few years after tagging, followed
by increasing retention rates over time. For loggerhead, there was no significant trend
between increasing tag age and probability of loss. This may have been affected by the lack of
remigrations by new breeders to the population resulting in a lower number of loggerhead
recaptures than green (Tucker, 2010). Titanium flipper tags are highly resistant to corrosion -
at least seven years with no corrosive damage (Limpus, 1992), and there have been few
observations at Alagadi of tags being damaged or lost as a result of corrosion. The non-toxic
properties of titanium tags can mean that barnacles form on the tags. This increases the
overall size and weight of the tag resulting in an increased probability of loss. In some cases,
barnacles cannot be easily removed and may deem the tag unreadable for a considerable
length of time. The main cause for titanium tag loss is likely to come from the tags self-locking
‘through the hole’ mechanism. Due to the lack of proficiency of inexperienced volunteers, or
those with a limited amount of strength, the piercing point is not always fully bent into the
lock of the tag. Greater titanium tag loss has previously been associated with loggerhead and
green at nesting beaches over feeding grounds (Limpus, 1992). Due to the vigorous digging
actions of females whilst nesting and multiple nesting attempts, it is most likely that
improperly attached tags will be lost within the first few years revealing initially high rates of
tag loss (Figure 1c and Figure 3c). This issue can be avoided by ensuring, for all tags, that the
piercing point has locked fully into place with the respective specific tag applicators. If the tag
is still not in fully locked, then pliers should be used to complete the procedure (Balazs, 1982).
As expected, for both species PIT tags had the highest retention rates of all tag types
and results show that we are far off reaching their maximum lifespan limits (Figure 1a, Figure
3a). As PIT tags are internal, they are not at risk to abrasion or corrosion. As with plastic dart
tags used in many other marine species (Kirkwood, 1981), PIT tags can become so firmly
imbedded and over grown by tissue, that as time passes the probability of loss becomes closer
to zero (Rivalan et al., 2005). One of the drawbacks for only using PIT tags to monitor turtle
populations is that fishermen are unable to detect and observe PIT tags on turtles they catch
– that is unless they have been provided with a universal PIT tag scanner. As PIT tags are known
to be permanent marking tags (Gibbons and Andres, 2004), it would be reasonable to
attribute low levels of PIT tag loss to faulty application rather than physical loss. PIT tag loss
could also be associated with failure to detect the tag – be this from failure of the tag itself
13
(Wyneken et al. 2010) or by inexperienced volunteers on patrol failing to detect the PIT tag
and replacing with a new tag. For 32% of green turtles and 31% of loggerhead turtles there
was a failure to read their PIT tag. Some of these failures resulted in the turtle being given a
new PIT tag (20% of greens and 32% of loggerheads). One female loggerhead was given four
new PIT tags over the course of the study as the previous PIT tags were not detected or had
failed to have been read. In recent years, all five PIT tags have been detected and read for this
individual showing that all the tags are still in full working order. In a study on hawksbill turtles,
van Dam and Diez (1999) found a 15% failure rate in the ability to detect PIT tags over 5years
showing that the results from this study are not negligible. The variation between the PIT
tagging proficiency of volunteers suggests that further efforts need to be made to standardise
training and tagging procedures (Shaughnessy, 1994).
PIT Tag Use
Tag loss estimates have been enhanced over the years by the use of permanent tagging
methods. In the present study, without the use of PIT tags, calculated estimates for flipper tag
loss for both green and loggerhead would be considerably lower (Table 1, Figure 1(b-d) and
Figure 3(b-d)). This was most apparent in green turtles (Figure 1) which suggests that almost
50% of all green turtle recaptures would result in incorrect neophyte identification (rather
than a returning turtle who has lost both her flipper tags).
Estimates of tag loss rates using permanent tagging methods are essential to reducing
bias in parameter estimates from population models. The use of PIT tags in Alagadi reduces
the uncertainty of incorrect neophyte identification (McDonald & Dutton, 1996). Without the
use of PIT tags, green neophyte numbers (2009-2015) would have been over estimate by
44.16% for green turtles and 24.50% for loggerhead turtles. Rising numbers of neophytes
within the population is indicative of population growth (Richardson et al. 2006). Results from
this study outline a vital question that all recapture projects must consider; if tag loss is being
underestimated, how much is recruitment and population size being overestimated? This
means that an over-estimation of neophytes number would result in an over-estimation of
population number (Stobo and Horne, 1994) leading to false assumptions regarding
population growth of loggerhead and green turtles at Alagadi. Survival estimates could
therefore also be biased as among capture-mark recapture models because an individual that
has lost its tags is no longer recognisable and so is indistinguishable from dead individuals. If
14
such bias is not detected and corrected for, any data collect for population monitoring will be
unreliable and invalid and we would see much larger recruitment estimates and
underestimation of survival for many populations. For example, the estimated annual flipper
tag loss rate calculated during a study on Californian Sea Otters (Enhydra lutris), led to
inaccurate and underestimated survival rates when data was derived from observations of
tagged individuals (Siniff and Ralls, 1991). Conservation efforts derived from such data may
not be relevant, or, at the very least, not as effective as they could be. For other marine turtle
projects, earlier estimates based solely on flipper tag returns should, where possible, be
revisited using permanent tagging methods in order to assess the accuracy of their tag loss
estimates. This will allow them to correct for any bias in their population monitoring data.
Double Tagging
Double tagging began as a way for monitoring projects to increase the chance that at least
one tag would remain on the turtle (Henwood, 1986). Tag loss is most often quantified using
double-tagging experiments that consist of releasing and monitoring groups of double tagged
animals and observing the proportion of animals that are recaptured with one or both tags
present (González-Vicente, 2012; Henry and Jarne, 2007; Dicken, 2006). This usually assumes
that the probability of losing one tag is independent of losing the other and so tag loss can be
estimated using animals that have lost one tag. There is a continuing body of evidence
showing that the assumption of independent tag loss is flawed (Schwarz et al., 2012; Rotella
and Hines, 2005; Rivalan et al., 2005). Using permanent markers, researchers are able to
determine the rate of loss for the second tag, whilst still being able to identify the individual.
A study on black bears using tattoos as a permanent marker found that the probability of a
male losing a second ear tag was greater if the first ear tag had already been lost (Diefenbach
and Alt, 1998). This had resulted in 6% bias for previously calculated annual survival estimates.
A more recent study on elephant seals found that there was 28% greater likelihood of an
individual losing its second flipper tag after the first tag had been lost (McMahon and White,
2009). In other words, if an animal is given two tags of the same nature (e.g. two flipper tags,
or two ear tags), it is more likely to lose both of its tags than it is to lose just one. At this point,
the extent to which this has affected the estimates for tag loss calculated in this study is
unknown, but should and will be addressed in future studies at Alagadi.
15
Between Species Variation
Sea turtles display obligate skipped breeding behaviour and lay a variable number of clutches
every few years. During inter-breeding periods they accumulate energy needed for
reproductive migrations and may only breed when their body condition and environmental
conditions reach a threshold value (Solow et al., 2002). Following tagging, 72.69% of
loggerhead and 38.74% of green turtles did not re-migrate to Alagadi in subsequent breeding
seasons. This suggests that green turtles are more faithful to their nesting beaches than
loggerheads (Phillips et al., 2014; Mortimer and Portier, 1989). A satellite telemetry study in
Florida showed that re-migrant loggerheads had higher site fidelity, compared to new
breeders (Tucker, 2010). This would suggest that the likelihood of recapturing a green turtle
after tagging is higher than the likelihood of recapturing a loggerhead turtle after tagging. This
could reflect some of the differences seen in the tag loss probability estimates for this study.
For example, there was a 0.244 difference in the mean probability of flipper tag loss with and
without the use of PIT tags for Green. For Loggerhead, this difference was much lower (0.100).
It would not be unreasonable to suggest that if more loggerhead neophytes did return, then
we would see even more accurate estimations for tag loss probabilities.
Other Tag Loss Concerns
Tag loss can result from a diverse range of causes. Flipper tags can be bitten by attendant
males biting at the flippers of mounted males during courtship (Limpus, 1992; Balazs, 1982).
If the tag is bent or squeezed against the flipper, this could lead to tissue degeneration
contributing to an increased probability of loss. In order to reduce the probability of tags being
lost for this reason, studies should use the smallest tags practical.
There have been many studies documenting the effects of tags on drag and
hydrodynamic efficiency in marine vertebrates (Serafy et al., 1995; Hazekamp et al., 2009). In
a study on penguins, the effect on drag caused by flipper bands resulted in higher energy
expenditure whilst individuals were in the water (Le Maho et al., 2011). This led to lower
foraging efficiency resulting in longer foraging trips and, ultimately, lower survival and
breeding success (Le Maho et al., 2011). No studies on the flipper tags used in this study have
found such effects on the hydrodynamics of green or loggerhead sea turtles. However,
biofouling, barnacles, debris and anthropogenic waste is known to sometimes attach to the
flipper tags of turtles, particularly when they have not been attached correctly. This increases
16
the weight and overall size of the tag and will contribute to an increase in drag. This will also
have serious effects on the turtle’s risk of entrapment and entanglement.
Marine turtle monitoring programmes must be cost effective in order to sustain data
collection over long periods of time. This will ensure they have enough data to draw accurate
estimations of populations and draw meaningful conclusions from studies. Variable funding
makes it difficult to ensure stability for these projects and so they should be based upon a set
of robust, inexpensive measurements that can be consistent long term (Lovett et al., 2007).
The cost of tags should be considered. Titanium flipper tags cost substantially less than PIT
tags (approximately US$2.20 per tag and $8.00 respectively). It is therefore important that
monitoring programmes consider the value of tags types based on the data that will be
obtained as well as the actual cost (Morely, 2002).
To conclude, tag loss can have profound effects within a population monitoring program. If
not appropriately assessed, tag loss errors will lead to over-estimation of population levels
and underestimation of survival rates. The use of permanent marking methods (such as PIT
tags) are invaluable in producing accurate estimations of tag loss. It is recommended that all
population monitoring programs undertake an assessment of tag loss alongside other data
collection to reduce any bias that may occur. A continued effort to develop and refine tag
types and tagging techniques across all species is important in reducing tag loss thus reducing
cost and increasing the quality of data collected.
Acknowledgements
Many thanks to my supervisor Annette Broderick. I would also like to thank the Marine Turtle Conservation Project field teams 1992-2015.
17
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21
Appendices Appendix 1: ethical approval
Appendix 2: risk assessment
DSE User Self-Assessment Form
Name of DSE User Kelle Holmes College / Service / Dept Date of Assessment 10/09/2015 CLES - Biosciences
DSE Component NO
YES Action Required /
Comments Desk
Is there enough space on your desk top for the flow of work?
1 Y
Have you got enough leg room? 2 Y Is the desk deep enough for you to have the monitor set between 450mm and 650mm from your eyes, when you are seated in the correct position?
2*
Y
Is there enough room for a space between your keyboard and you for your wrists to rest on the desk (4-6 inches / 10-14cm recommended) between typing
2*
Y
Is your desk surface free from reflection? 1 Y Chair
Is your chair at a height where the bottom of your elbows are at the same height as the keyboard when using the keyboard?
2 Y
Does the back rest support the small of your back in an upright posture?
1 Y
22
DSE Component NO
YES Action Required /
Comments Can you sit back into the chair seat fully without any pressure behind the knees?
2 Y
If fitted, are armrests set up correctly i.e not preventing adequate movement of the chair?
1 N/A
Can you get close to the desk to type with the elbows vertically under the shoulders?
2 Y
Is the chair comfortable? 1 Y Is the chair stable and all adjustment levers working? 2 With seat height adjusted correctly for the elbows, can you place your feet firmly on the floor without compressing the underside of your thighs?
2 Y
If a footrest is required, have you got access to one? 2 N/A Footrest not needed Monitor
Is the monitor / screen between 450mm-650mm away from your eyes (arms length)
2 Y
Is the monitor directly in front of you? 2 Y Are your eyes level with the top of the screen? 1 Y Is the screen free from glare / reflections? 2 Y Close curtains, alter angel
of lighting Is the information on the screen well defined and easy to read?
1 Y Use font size 11 or higher
The image is flicker free? 2 Y Do you clean the screen regularly? 1 Y Is the monitor tilted between 5 and 15% off the vertical? 1 Y Can you adjust the brightness and contrast easily? 1 Y
Keyboard Is the keyboard at the correct angle to prevent any up or down bending of the wrist?
2 Y
Is your keyboard far enough away from you to ensure your elbows are directly under your shoulders when typing?
2 Y
Do you always move your keyboard out of the way when you are using only the mouse?
1 Y
Is the keyboard clean? 1 Y Are the digits clear and not faded? 1 Y
Mouse Is the mouse close enough to avoid extending the arm at the elbow?
2 Y
If you have a roller ball mouse (laser mice do not need a mouse mat), do you have a mouse mat?
1 N/A Laser mouse being used
Does the mouse run freely on the mat and work accurately?
1 Y
Do you regularly clean your mouse and internal mouse ball?
1 Y
Do you reduce the time using your mouse to the lowest period possible by using keyboard short cuts?
2 Y
Document Holder Do you have a document holder (if required)? 1 N/A Not required Can you refer to documents and papers without having to move your head?
1 Y
23
DSE Component NO
YES Action Required /
Comments Other Equipment
Is all equipment and items around you necessary? (or can it be removed to give you more desk space?)
1 Y
Is all other equipment (phone etc) in a position to ensure that you can maintain your posture when using them?
1 Y
Space and environment Can you move in and out of your workstation easily? 2 Y Is there adequate space to manoeuvre your chair?
2* Y
Is the area free from trailing cables which pose a trip hazard?
2 Y
Is lighting adequate? 2 Y Do windows have blinds to prevent glare and reflection? 1 Y Do you find the work station quiet enough? 1 Y Is the temperature comfortable for most of the time? 1 Y
Are you free from any upper body pain/soreness or any soreness in your hands or wrists
2*
Y
About You Have you had an eye test in the last 2 years? Please follow this link to eye test information
2 Y Summer 2014
Do you organise your work to ensure you take a 5 minute break for every hour you are using the DSE?
2 Y Regular breaks away from DSE
Is your workstation set up to ensure that you have a flow of work (you don’t have to keep getting up or twisting for things)?
1
Y
Do you feel you understand and can effectively use all of the computer programmes you have to use as part of your job?
2 Y
Do you have an existing medical issue that you feel is being aggravated by your workstation?
N Y* score
2
None
Do you suffer from dry or sore eyes when using your DSE? N Y* score
2
None
Do you feel you require extra DSE information or training? N Y* score
2
none
Total Score 2
Action Plan
Actions Required Responsible Person
Date for Completion
Copy of the DSE assessment must be sent to Line Manager. Place in personal file.
DSE USER IMMEDIATE
Date set for next assessment (annual re-assessment required) N/A