Study area and ringing data
Oystercatchers have been fitted with colour rings in more than 30 ringing areas within the Netherlands, including the Wadden Sea estuary which is located in the north of the Netherlands, the Dutch Delta estuary which is located in the south-west of the Netherlands, and during the breeding season in several inland locations (Fig. 1a–c). Colour-ringing projects were restricted to the Wadden Sea islands of Ameland, Schiermonnikoog and Texel prior to 2008 but expanded to include the Dutch Delta and inland areas from 2008 onwards. Ringing operations have principally been performed during summer when oystercatchers can be caught on the nest, although oystercatchers have also been caught during winter using cannon or mist nets.
An engraved colour-ring was fitted to both the left and right leg (tarsus), and a non-engraved colour marker was also attached (tibia) together with a standard metal ring (Fig. 1c). The engraved rings generally consist of two layers, the outer layer consisting of the coloured material which is engraved to a depth that exposes the inner layer which is either black or white (Rees et al. 1990; Ward 2000). The material of the inner layer may vary, for example Ward (2000) described Perspex or other acrylic plastics whilst one of the leading suppliers for Europe (Interrex; www.colour-rings.eu) described a multi-layered impact acrylic (PMMA) material. Manufacturing practices have changed over time, not only in the material used but also in ring thickness and the depth of engravings (Rees et al. 1990). Unfortunately, the history of rings used during our study has not been recorded and hence we were unable to investigate ring wear in relation to the ring material. The non-engraved colour marker may be one of four colours, black, green, red or yellow. The engraved rings may be one of eight ring colours, including black, blue, green, lime, orange, red, yellow and white, and were engraved with one of 17 letters (A, B, C, E, G, H, J, K, L, N, P, Q, S, T, W, Y, Z). The engraved rings on the left and right leg would have a different colour each (i.e. not the same colour on each leg) but the letters could be the same (e.g. Left = red A, right = yellow A). The legs of adult oystercatchers may vary in colour from a pinkish to a more reddish hue, whilst the colour of juvenile’s legs is blue-grey. Researchers on Schiermonnikoog use colour rings with a barcode system (Fig. 1b). The barcode system may be more difficult for citizen scientists to learn, but from greater distances the barcode is easier to decipher once observers become accustomed to the ring style (pers. obser.).
Our analysis focuses on observations made between 2008 and 2017, but includes individuals that were ringed prior to 2008. The reason we focus our analysis from 2008 onwards is that the volunteer outreach project in 2008 coincided with the launch of a website called Wadertrack (www.wadertrack.nl) which provided a portal to enter observations of colour-ringed oystercatchers. At a minimum, the web-portal records the ring information, the co-ordinates of the observation and the date of the observation. A graphical help tool is built into the website to help observers generate the required colour code whereby the observed colour-markers can be dragged onto the appropriate parts of the leg and hence reduces the risk of incorrectly reported colour-codes. Additional information about the observation can also be provided, and importantly this included a data field where the condition of the rings could be noted. The options include no wear, worn but easy to read, worn but hard to read, ring lost and ring moved (e.g. if a ring moves from the tibia to the tarsus). However, the ring condition applied to all rings and it was not possible to report the status of each ring separately, i.e. the information was only collected at the individual level. Therefore, we do not distinguish between individuals that have worn/lost one, two or three rings, but instead, we define an individual to have a lost/worn ring when any ring has been lost or worn. In addition, in the event of a lost or worn ring, a data field was also available to enter the number of the metal ring (complete or partial). In total, 7069 oystercatchers were ringed between 2008 and 2017, and an additional 1840 oystercatchers were observed between 2008 and 2017 that were ringed prior to 2008. In total, 118,071 observations were made between 2008 and 2017 of 7469 colour-ringed individuals (Table 1) and 2.3% (n = 2808) of observations were not matched to an individual in our database for reasons that include observations of internationally ringed birds (e.g. UK, Denmark, Iceland etc.), incomplete colour codes which may be due to ring loss, wear or the observer was unable to read all the rings, or potential errors made when reading the ring.
Rates of ring wear and loss
We examined the information provided on Wadertrack to estimate approximate rates of ring wear and loss. We also identified all observations that were incomplete and by using the information provided on Wadertrack, we determined whether the incomplete observation was due to ring wear/loss or observation-related challenges (e.g. roosting oystercatcher on one leg or poor weather conditions). In many instances, even though a ring may be heavily worn or lost, an individual could be identified by the metal ring or another identifiable feature, for example fidelity to a certain area or a morphological feature like an unusual plumage or leg deformity. Therefore, to estimate the number of individuals with worn/lost rings, we included both individuals that could be identified (i.e. Known IDs) and also incomplete observations that report a worn or lost ring but the individual could not be identified (i.e. Unknown IDs). Distinguishing between Known and Unknown IDs provides an indication of the proportion of birds with worn/lost rings that are identifiable. Furthermore, the same individual may be reported on multiple occasions, for example if one observer is able to read a metal ring (thus Known ID), whilst a second observer is only able to read the colour rings and thus provides an incomplete observation (Unknown ID). Unknown IDs may also contain multiple observations of the same individual, given that we cannot distinguish between two observations of one bird with a lost ring, or two observations of two birds with lost rings. Hence, including Unknown IDs likely provides an overestimate of ring wear/loss and thus provides a precautionary approach for estimating the scale of ring wear and loss.
We related the number of individuals reported with a worn or lost ring for the first time to the cumulative number of colour-ringed individuals to estimate the annual reporting rate of ring wear or loss (alpha; Table 2). We also corrected the cumulative number of ringed birds with an annual survival of 90% to incorporate mortality in the population (Table 2; Ens and Underhill 2014). To avoid potential distortions resulting from variation in survival amongst adults and juveniles, we only included birds ringed as adults in the analysis (n = 4206). When an individual had a worn or lost ring, we only included the first year that the ring was reported worn or lost to avoid multiple entries for the same individual. In a mark-recapture analysis, a heavily worn or lost ring would often mean that an individual becomes non-identifiable and hence a perceived mortality (Juillet et al. 2011). Since an individual can only be perceived to die once, we did not want to bias our estimates for rates of ring wear and loss by including multiple entries of ring wear/loss for the same individual. However, it is likely that resighting rates of birds with worn rings were higher than lost rings. Therefore, if a bird first had a worn ring, and then later a lost ring, both entries were included in the analysis, for example, if a ring was reported worn in 2012, and then lost in 2015, both would be included in the analysis. However, if a bird first lost one ring, and then it lost the other ring, we did not include a second entry since the individual would already belong to the “lost ring” category.
Future observations of individuals with worn/lost rings
We performed two additional analyses for oystercatchers that were known to have a worn or lost ring. In both analyses, we identified the first observation where an oystercatcher was reported with a worn or lost ring. The first analysis removed all subsequent observations made by the observer that first reported the ring as lost or worn. We then estimated the proportion of oystercatchers that were resighted even though the ring was worn/lost (beta; Table 2), and of the resighted individuals, did other observers also report that the colour ring was worn or lost (epsilon; Table 2). The first analysis focuses on whether an individual oystercatcher was reported by other observers, but an oystercatcher could be resighted ten times but only be reported with a lost ring once. Therefore, in the second analysis, we performed our analysis at the observation-level and estimated the proportion of all future observations that also reported the ring as worn/lost (gamma; Table 2). Some individuals (n = 42) had the worn/lost ring replaced hence we only focused on observations between the date that a ring was first reported worn/lost and the date that the ring was replaced.
Probability of ring wear and loss
We estimated the probability that an oystercatcher was reported with either a lost or heavily worn colour-ring in relation to the age of the ring (years since the ring combination was fitted) and the colour of the ring (theta; Table 2). We performed the analysis using a generalised linear model (GLM) with a binomial response of either 1 = ring worn or lost, or 0 = ring not reported worn or lost and fitted an interaction term (*) between the colour of the ring and the ring’s age. We only included resighting data up to and including the year that an individual was first reported with a worn or lost ring to avoid complications resulting from observers not including information about the condition of the ring (e.g. a ring may be reported lost in 2012, but not in 2013, even though the ring was known to be lost, which would consequently skew probability estimates of the binomial model). In addition, some individuals had their rings replaced when they became worn or lost. In some instances, these were easy to identify because the individual received a new ring combination, and thus the age of the individual’s ring combination would reset to zero. However, information was not recorded if an individual’s rings were replaced with the same combination and thus the age of the ring combination may not accurately reflect the true age of the rings. Our analysis only focused on the engraved rings and excluded the colour markers on the tibia (Fig. 1; Additional file 1: Appendix A). Since all individuals (excluding those with barcode rings) have an engraved colour-ring on both legs, and generally it was not recorded which colour-ring had been lost or was worn (some citizen scientists included information in a comments field), we replicated the data so that the colour-rings from both legs were included in the analysis (i.e. each individual had two entries). Including the rings from both legs would ensure that all ring colours were evenly represented. To verify our approach of combining rings from both legs, we performed two additional analyses (Additional file 1: Appendix A). Instead of combining the rings from both legs, we analysed ring wear and loss for each leg, the results of which are described in Additional file 1: Appendix A. In a second analysis, we only included individuals where the lost or worn ring was known, although this resulted in a much reduced sample size (Additional file 1: Appendix A).
We also estimated how habitat may influence the probability of ring wear and loss, although we defined habitat by describing three broad areas within which individuals were ringed. Our areas were the Wadden Sea, Inland and the Delta (Fig. 1). All individuals were classified to an area based on the ringing location (Table 1). Inland birds largely forage in grasslands during summer but will migrate to coastal regions during winter although in many instances the wintering location is unknown (Allen et al. 2019). Oystercatchers are frequently observed foraging on oyster beds and stone dikes in the Delta region, which may damage rings, especially on the tarsi. The Wadden Sea is a large inter-tidal area of mudflats with a diverse array of habitats within which oystercatchers may forage. We considered models with habitat alone, and with habitat as interaction term with time and/or ring colour, and selected the top performing models based on AIC.
Resighting probability of ring colours
To investigate colour-specific ring wear, we determined whether resightability varied amongst ring colours in a mark-resighting analysis with individuals divided into groups according to their ring colour. Note that an individual may belong to two groups if it had two different engraved colour-rings, which most individuals had. Since ring colours on each leg were not independent (i.e. the detection of one ring may be influenced by the colouration of the ring on the other leg), the resighting probability may be influenced by the ring combination. Therefore, in addition to a model structure that contained each of the eight ring colours independently, we also included a model structure with the ring combination to identify general patterns of detectability, for example whether ring combinations of yellow/black have a different resighting rate than yellow/red (Additional file 1: Appendix B). Researchers on Schiermonnikoog use a bar-code system for rings which we did not divide by colour but instead group this class of rings as “Barcode”. The sampling period was from April to June inclusive, when oystercatchers are on their summer breeding ranges. Although mark-recapture models are generally designed for instantaneous sampling, a large portion of our data would be lost if we excluded citizen science observations. Therefore, we used a non-instantaneous sampling design, with observations collected over a three-month period. Previous research has indicated that mark-recapture models can be robust to violations of the assumption of instantaneous sampling, and non-instantaneous sampling may actually improve the precision of results (O’Brien et al. 2005). In the mark-resighting analysis, we considered model structures that either held resightings and survival constant over time or allowed these to vary over time. We performed the analysis in Program Mark (White and Burnham 1999) but developed the model using the package RMark (Laake 2013) in R 3.4.1 (R Core Team 2017).
Mark-resighting simulation of ring loss
To quantify how ring loss may impact mark-recapture analyses, we created and simulated four scenarios of ring loss and resightings that replicated the results of our study. We randomly generated a dataset that simulated survival over a ten-year period for 1000 individuals with 90% survival (Ens and Underhill 2014). The 1000 individuals were introduced as a single cohort on the first occasion. We then simulated ring loss such that each year, living individuals had a 2.5% probability of losing an engraved ring. In the simulation, individuals that had lost a ring could not lose another ring. We subsequently generated an observation table whereby living individuals with complete rings had a 70% resighting probability whilst we generated four scenarios for individuals with lost rings as follows:
Business as usual—replicates a scenario in which birds do not lose rings, i.e. resighting probabilities of birds with lost rings equalled those with complete rings
Complete loss—birds with lost rings are never resighted
Partial resightability 1—all individuals are identifiable, and assuming an individual was resighted (70% probability), it could only be identified 50% of the time due to the lost ring
Partial resightability 2—50% of individuals with a lost ring are never resighted and identifiable individuals had a 70% resighting probability
Scenarios three and four compared two mechanisms for how individuals with lost rings may be observed by citizen scientists in the field. The differences may appear subtle, but the implications for a mark-recapture analysis may vary between the two scenarios. As an example, in scenario three, two individuals (A1 and A2) with lost rings will have an equal resighting probability (70%). Hence, over ten years of sampling, both birds are observed seven times but because of the lost ring, only 50% of the observations were identifiable (3.5 times). In scenario four, using the same two individuals (A1 and A2) but now individual A1 is never resighted during the entire 10 year study period because of the lost ring, whilst individual A2 has a 70% resighting probability and individual A2 is identifiable despite the lost ring.
We generated a mark-recapture history for these four scenarios and performed our analysis using the Cormack-Jolly-Seber mark-recapture model in Program Mark (White and Burnham 1999), through RMark (Laake 2013), to compare estimates for the survival and resighting parameters of each model scenario. To validate the simulation, we compared models with time-varying survival and resighting probability, however since we kept survival (90%) and resighting (70%) constant, the time independent model should perform best.