PIT tagging does not measurably reduce reproductive success in sensitive burrow-nesting seabirds

PIT tagging does not measurably reduce reproductive success in sensitive burrow-nesting seabirds | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Research Article PIT tagging does not measurably reduce reproductive success in sensitive burrow-nesting seabirds Léo Marcouillier, Eliane Miranda, Shannon Whelan, Dave Fifield, and 4 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-3112880/v1 This work is licensed under a CC BY 4.0 License Status: Published Journal Publication published 22 Feb, 2024 Read the published version in Marine Biology → Version 1 posted 5 You are reading this latest preprint version Abstract Investigator disturbance while monitoring seabirds often results in lower survival rates and breeding success, leaving lasting negative impacts on the population and biased observations. Puffins, in particular, are more sensitive to investigator disturbance than many other seabirds, and researchers must seek to decrease their disturbance and time spent at puffin colonies. Radio-Frequency Identification (RFID) via Passive Integrated Transponder (PIT) tags is an inexpensive and reliable way to identify individuals when coupled with automated RFID detectors, potentially avoiding the need for recapture for nocturnal seabirds. PIT tags either can be implanted subcutaneously or attached externally to leg bands, but it is unclear which method causes lower disturbance. To examine the impact of PIT tagging on rhinoceros auklets ( Cerorhinca monocerata ; a member of the puffin clade) nesting in artificial burrows on Middleton Island, Alaska, during the 2022 breeding season, we monitored burrow entrances with automated recording RFID readers to collect presence and nest attendance data. PIT tagged and control birds had similar breeding success and chick growth rates. Birds tagged externally were detected less often than birds marked with a subcutaneous implant. We conclude that PIT tagging on the rhinoceros auklet is a relatively non-invasive method for seabird monitoring, and that subcutaneous implants doesn't cause more disturbance than external attachment. Figures Figure 1 Figure 2 Figure 3 Figure 4 Figure 5 Figure 6 Figure 7 INTRODUCTION The uncertainty principle in field ecology states that an investigator will always disturb the behavior of the biological model they are studying (Lenington 1979 ). Investigator disturbance and its consequences are widely studied in field ecology (Hockin et al. 1992 ; De Jong and Hoback 2006 ; Carey 2009 ). For example, observing avian behavior via biologging can induce higher mortality and nest predation (Ibáñez-Álamo et al. 2012 ), reduced breeding success (Sandvik and Barrett 2001 ; Blackmer et al. 2004 ) or abnormal behaviors (Brown and Morris 1995 ; Burger 1998 ). While these effects do not always interfere with the traits of interest (e.g., morphology), investigator disturbance can clearly bias estimates of important life history traits. Using Radio Frequency Identification (RFID) presents a potential solution to reduce disturbance on monitored seabirds while measuring patterns of nest attendance behavior (Tyson 2021 ). Individuals can be equipped with Passive Integrated Transponders (PIT) tags that are small and can be attached quickly without, for example, soiling feathers. It allows for the identification of marked individuals, improving resighting data collection through automated networks without the need for recapture for band-reading (Gibbons and Andrews 2004 ; Bonter and Bridge 2011 ). The technology is used on a variety of taxa and increases the general knowledge on population dynamics of multiple species by providing strong estimates of survival and recruitment rates (Rebke et al. 2010 ; Sutherland and Dann 2012 ; Horswill et al. 2014 ). These demographic parameters can inform predictive models to fine-tune conservation plans depending on the different constraints a population is facing (Weller et al. 2014 ). Puffins ( Fratercula and Cerorhinca spp.) , show strong responses to their environment through breeding success and foraging behaviour (Bost and Le Maho 1993 ; Gjerdrum et al. 2003 ; Sydeman et al. 2017 ). However, puffins and other burrow-nesting auks are notably hard to study because of their high sensitivity to human disturbance (Rodway et al. 1996 ; Whidden et al. 2007 ; Elliott et al. 2010 ; Harris and Wanless 2011 ; Sun et al. 2020 ; but see Kelly et al. 2015 ). Rhinoceros auklets ( Cerorhinca monocerata ) are burrow nesting puffins that are mostly active on their colonies at night. Nocturnality makes the collection of observational data challenging, as color bands cannot be easily read from a distance, resulting in knowledge gaps for the species ecology. Rhinoceros auklets exhibit breeding site fidelity (Kubo et al. 2018 ) making them a good target for long-term monitoring. However, executing such studies requires accessing burrows regularly, accelerating habitat destruction (Priddel and Carlile 1995 ). Such practices can have strong deleterious effects on the long term (Wilson 1986 ), increasing the risk of burrow collapsing as well as reducing their breeding success through higher nest abandonment rates. Given the sensitivity of some burrow-nesting seabirds, especially puffins, to human impacts (Watson et al. 2014 ; Sun et al. 2020 ), our objective was to set up a minimally invasive protocol for the long-term monitoring of rhinoceros auklets on Middleton Island, Alaska, through automatic Radio Frequency Identification (RFID). We used an experimental approach to test the effects of different PIT tagging protocols on nest abandonment probability by tagging birds (i) at different times of the breeding season (late incubation vs early chick rearing), (ii) externally and internally (subcutaneous implantation in the neck vs external attachment on a 3D-printed leg band) and (iii) at different intensities (single vs both adults in burrow tagged). We detected individuals using automatic RFID readers. We were particularly interested in whether breeding stage impacted abandonment rates, as some studies (Sun et al. 2020 ) but not others (Kelly et al. 2015 ) have documented increased abandonment during incubation, when adults are presumably less invested in their offspring because their subsequent survival is lower (i.e. chicks necessarily are more likely to survive to fledging than eggs). We were also interested in whether leg-mounted or internally implanted PIT tags would cause less abandonment, as leg-mounted devices can alter flying and diving behavior due to imbalanced distribution of weight and buoyance but implanted tags may cause infection (Hatch et al. 2000 ; Elliott et al. 2007 ; Vandenabeele et al. 2014 ). This method provided an opportunity to learn more about cryptic nest attendance behavior. METHODS Study system We collected data from rhinoceros auklets breeding in a colony on Middleton Island, Alaska (59.42° N, 146.32° W). The colony has been monitored since 1977 and diet and population metrics are collected annually since 1993. During the breeding season (April to August), this population of rhinoceros auklets nest in burrows dug in soil slopes dominated by salmonberry bushes ( Rubea spectabilis ). Nest attendance patterns and sensitivity to human disturbance differ between incubation and chick-rearing (Sun et al. 2020 ). Parents are more likely to abandon the nest after human disturbance in the early stages of breeding. Breeding pairs lay a single egg in late April to early May and incubate for approximately 45 days. During incubation (and the first days of chick rearing), the parents typically take turns incubating the egg (or hatchling) for two days shifts. Parents will then both cease daytime burrow attendance and spend the daytime foraging at sea, returning to the colony once each night to feed the chick by delivering a “bill load”. These deliveries tend to include multiple prey items (usually fish) carried between the mandibles and dropped inside the nest chamber of the burrow (Gaston and Dechesne 1996 ; Davoren and Burger 1999 ; Kato et al. 2003 ; Cunningham et al. 2018 ). This phase lasts around 50 days until the chick fledges and leaves the nest (Harfenist and Ydenberg 1995 ). We conducted this study using artificial nest boxes. Between 2017 and 2021, 121 artificial nest boxes were installed in a limited area within a breeding colony of rhinoceros auklets on Middleton Island. The artificial burrows consist of two parts: A L-shaped wooden box made in ½-inch-thick plywood treated with wood preservative and a corrugated plastic tubing as entrance tunnel (Fig. 1 ). The top of the box is equipped with a trap door for easy access to the nesting chamber. The nest box floor is made of wire mesh. The nest box is buried in the ground, partially filled with soil, and then marked with a uniquely numbered stake to be easily re-located. Reproductive success monitoring We checked nest boxes for the first time in 2022 on 20 May. We examined the boxes for the presence of an adult with an egg and floated eggs to estimate laying date (see below). We visited occupied nest boxes on May 30 and every 5 days thereafter until hatch to monitor breeding parameters (incl. hatching success, hatching date, chick survival and growth). At each visit, we recorded presence or absence of an adult and the temperature of the egg (cold or warm, indicative of how recently an adult was incubating). We measured chick weight (g) and wing chord (mm) 5 and 20 days after they were first found. Chicks were not disturbed between these checks. A breeding attempt at a nest box was considered successful (breeding success = 1) if the chick fledged. We checked for the presence of a live chick every 5 days, 45 days after the chick was first recorded as hatched. A chick was considered a successful fledgling if it was absent from the burrow during one of those post-45 day checks. The breeding attempt was considered unsuccessful (breeding success = 0) if the egg was found cold on three consecutive checks, or the chick was found dead or missing before the second measurement (no chick was found dead after 45 days). Most failure resulted from the parents abandoning the nest. When a nest box was checked, the entrance was plugged to prevent the adult from escaping and potentially abandoning the nest. The lid of the nest box was cracked open to see its contents. If necessary, we checked manually for the presence and temperature of a chick or an egg. During productivity checks, birds in nest boxes which had potentially been PIT-tagged before (see “PIT-tagging”) were read using a handheld reader (RT100V8, RealTrace, ATRIA Trading SA, Le Parray en Yvelines, France) . If the bird showed signs of stress, we tried to feel its metal band instead to limit disturbance and abandonment risks. For similar reasons, we skipped nest boxes on productivity check days if one of the birds inhabiting the box had been tagged less than three days prior. Floating height and angle are good predictors of the laying date (Liebezeit et al. 2007 ). To estimate laying phenology, we used the flotation technique described in Sun et al. ( 2020 ) for rhinoceros auklets at our study site by measuring either the angle that eggs rested (sinking eggs) or the height of exposed egg above water (floating eggs). For a sinking egg, we used the equation: $$\begin{array}{c}Days until hatch=46-\left(0.002*floating angl{e}^{2}+0.078*floating angle+1.16\right) \#\left(1\right)\end{array}$$ For a floating egg: $$\begin{array}{c}Days until hatch=46-\left(2.014*floating height+20.027\right) \#\left(2\right)\end{array}$$ PIT tagging We found 63 occupied nest boxes on the first check. These nest boxes were assigned a treatment (Control, Late-incubation, or Chick-rearing). We assigned 20 nest boxes each to the Late-incubation and Chick-rearing groups: 10 boxes with a single adult tagged and 10 boxes with both adults tagged for a total of 60 birds with a PIT tag. Half of the birds were PIT-tagged subcutaneously in the neck and the other half were banded on one leg with a special plastic band 3D-printed to hold a PIT tag. The remaining 23 nest boxes were assigned to the control group. Treatment groups were assigned to be balanced across phenology and space. Tag position (neck or leg) and number of adults tagged per nest box (one or both) were assigned via a random number generator. Three nest boxes in the chick rearing treatment group were excluded because the egg never hatched. Burrows assigned to the Late-incubation treatment were tagged 10 days before the estimated date of hatching. Chick-rearing birds were tagged as soon as they were found with a chick. If a chick was found without a parent during a productivity check the nest box would be checked every night for one week until the parent was found. If an individual was marked less than three days before the next productivity check, its burrow was skipped during this check to reduce disturbance. In one burrow, an individual not found after one week of marking effort was excluded from the study. Birds were marked with 12-mm EM4102 PIT tags (frequency = 125kHz). The PIT tag was either placed in a 1.25-mm thick 3D-printed nylon leg band on the left leg, and secured with super glue and Tesa tape (tesa tape inc. 5825 Carnegie Boulevard, Charlotte, North Carolina 28209), or inserted in the lose neck skin between the scapulae (Fig. 2 ). A single-use needle was used for each bird. The PIT tag was sterilized in a chlorhexidine solution overnight and then stored in PBS solution until injection. The injection point was disinfected with a cotton ball soaked in 70% isopropyl solution to part the feathers. The same cotton ball was applied on the wound for several seconds after the injection to prevent the tag from falling out during the closing of the skin around the puncture wound. Tagged birds were also banded with metal U.S. Fish and Wildlife bands on the right leg. The first tagged bird in each nest box had a small piece of Tesa tape wrapped around the metal band. This facilitated rapid identification during productivity checks as well as the monitoring of tag failure rates (e.g., the PIT tag leg band would fall off or the implant would migrate in the body/not be detectable anymore). When the bird was caught, its head was placed in a bag to reduce stress. The bird was released in the nest box from the tunnel immediately after being PIT tagged and the entrance was kept plugged for at least 5 minutes to prevent early abandonment. Capture and release time were recorded. Every late incubation bird (n = 30) and 10 chick rearing birds were tagged in the morning between 09:00 and 13:00. The 15-remaining chick rearing birds were tagged at night between 23:00 and 04:00. Implanting a PIT tag in the neck took 6 min 44 s (SD: 2 min 33 s) attaching a leg band equipped with a PIT tag took 4 min 8 s (SD: 1 min 7 s) Automatic PIT tag reading Loggers used custom-built automated, low-powered PIT tag readers. The device is made of two parts. The first is a custom designed 9.5cm x 8cm circuit board that holds a microcontroller, an internal clock and the memory that stores the record of every PIT tag reading. The circuit board was secured in a pelican case with silica gel inside to protect it from humidity. The second part is the antenna which is made of a copper wire coiled around a 3D-printed flexible ring dipped in Plasti Dip (Plast Dip International, 3920 Pheasant Ridge Drive Blaine, MN 55449) and wrapped in electrical tape. The diameter of the antenna measures 130 mm which fits the internal diameter of the nest boxes’ access tunnel. When powered, the antenna induces a magnetic field. To constrain its magnetic field frequency to the desired value of 125 kHz, the circuit board regularly reads the actual frequency of the magnetic field induced by the antenna and switches capacitors of appropriate value into the circuit to correct for frequency drift. When a PIT tag goes through the antenna, the magnetic field is disturbed which is detected by the circuit board, leading to a record. Each time the PIT tag is detected, its unique ID, the date and time are logged. The system was powered by a 12-V marine deep-cyle battery (model SCS225; Trojan Battery Company 12380 Clark Street Santa Fe Springs, CA 90670) connected to a battery charger connected to a 120-V power source, therefore allowing for complete autonomy the whole season. Power was distributed to multiple burrow monitors by a 16-position terminal block (OONO MD-D1349P-1, https://czh-labs.com/products/screw-mount-2x16-position-screw-terminal-block-power-distribution-module-1280 ). The power station was positioned at the entrance of the colony and was protected from the rain using plastic covering. The power station and the PIT tag readers were connected with 30-m cables allowing us to reach a major part of the colony. The readers were then spread in the colony and set up at the nest boxes (Fig. 3 ). The antennae were placed as parallel as possible to the access tunnel to reduce disturbance to individuals accessing the burrow and to maximize detection probability. We had 12 working readers. Every week, we changed the position of the reader to be able to monitor as many burrows as possible during the season. Every occupied burrow as well as 2 burrows where the chick disappeared from the nest were monitored with readers. This represented 27 boxes and 38 birds (15 tagged in the neck and 23 tagged on the leg). Statistical analyses All statistical analyses were completed using R version 4.0.2 (R core team 2020). We tested the effect of different aspects of PIT tagging on abandonment with binomial generalized linear models using a chi squared significance test. All interactions were first considered unless specified. If the highest rank interaction term was not significant, it was removed until only significant interactions and/or single terms remained. The effect of PIT tag location, number of adults PIT tagged, and breeding stage on abandonment were tested on the subset of PIT tagged birds. We compared the breeding success of control and PIT tagged rhinoceros auklets depending on their breeding stage (incubation or chick rearing) with Fisher’s exact test. A statistical power analysis was then run on the three following comparisons: breeding success of PIT tagged vs control individuals, individuals marked on the leg vs subcutaneously and individuals marked during incubation vs chick rearing with the R package “pwr”. The effect of PIT tagging on chick daily wing growth and weight gain was tested with an ANOVA. Given the flotation technique is only accurate within about 10 days, we used the following estimate for hatching date: $$\begin{array}{c}Hatching date=\frac{\left(Date chick first seen\right)-\left(Date egg last seen\right)}{2} \#\left(3\right)\end{array}$$ However, we kept the egg flotation estimate (1) or (2) when the egg didn’t hatch. We investigated differences in attendance pattern (number of detection.night -1 , timing of the first and last detection) depending on the position of the tag and how advanced the breeding season was with linear models using a random effect on individual ID to control for inter-individual variation. When an individual was recorded only once during a particular day, this record was removed from the colony presence analysis. To determine whether the position of tagging influenced the detection probability, we ran a capture-mark-recapture (CMR) analysis on the subset of marked individuals. We used one week of capture history from 33 birds detected between 15 July and 7 August (example of detection record in appendix A). The analysis was completed in MARK version 9.x (White and Burnham 1999 ). This was done via standard live encounter mark-recapture models (Lebreton et al. 1992 ), where the probability of an individual being seen is defined by 2 parameters: the probability the animal survived and remained in the sample area (ϕ), and the probability that the animal was encountered (p), conditional on being alive and in the sample area. Following Lebreton et al. ( 1992 ) methods, we began with a general model and examined simpler alternatives. Model selection was based on Akaike’s Information Criterion (AIC). The model with lowest AIC being considered as the most parsimonious one. The parameters estimated from the best model are given with 95% confidence interval (95% CI) computed from the Hessian matrix. RESULTS In total, 55 birds were PIT tagged in 37 different artificial burrows (Table 1 ). Table 1 Number of artificial burrows in each treatment group: Control (0 parent tagged), Single (1 parent tagged), Double (both parents tagged), depending on their breeding stage (Incubation vs Chick rearing) Late Incubation Chick Rearing Control 23 Single 10 (5 on leg, 5 in neck) 9 (3 on leg, 6 in neck) Double 10 (5 on leg, 5 in neck) 8 (5 on leg, 3 in neck) Among the 63 boxes we monitored, 52 successfully hatched an egg (82%) and 43 of the chicks fledged, which made an overall breeding success of 68%. Some chicks were still present in the burrow for the last productivity check on 13 August 2022. These chicks (Age ± SD = 50 ± 8 d, n = 22) were considered as successful fledglings. This assumption is reasonable since the probability of not being fledged on the last check depended on the age of the chick (Chi square test, χ21 = 6.59, p = 0.01) and not the treatment group (Chi square test, χ22 = 4.59, p = 0.10). PIT tagging did not significantly influence egg hatching success (Chi square test, χ21 = 0.52, p = 0.47) nor chick fledging (Chi square test, χ21 = 1.02, p = 0.31). Overall, we observed similar breeding success of control birds and birds PIT tagged during incubation or chick rearing (Fisher’s exact test, all p > 0.8). In addition, control individuals, as well as individuals tagged on the leg or in the neck had a similar breeding success (Fig. 4 ). PIT tagging of adults also had little effect on chick development, daily wing growth (ANOVA, F(2,39) = 2.69 p = 0.0807) (Wing length.day -1 ± SD = Control group: 2.4 ± 0.56 cm.day -1 , n = 16, one individual tagged: 2.9 ± 0.62 cm.day -1 , n = 15, both individuals tagged: 2.4 ± 0.75 cm.day -1 , n = 11) or weight gain (F(2,39) = 0.38 p = 0.69) (Mass.day -1 ± SD = Control group: 6.9 ± 1.6 g.day -1 , n = 16, one individual tagged: 7.4 ± 2.2 g.day -1 , n = 15, both individuals tagged: 7.2 ± 1.6 g.day -1 , n = 11). Breeding success was not related to PIT tagging on the subset of tagged birds (n = 37 boxes). The position of tagging (leg or neck) (Chi square test, χ21 = 0.18, p = 0.67), the number of birds tagged in the pair (Chi square test, χ21 = 1.49, p = 0.22) and breeding stage (Chi square test, χ21 = 0.56, p = 0.46) did not influence abandonment (Table 2 ). Table 2 Proportion of pairs that successfully fledged an offspring for each group Treatment n Number of successful pairs Percentage of successful pairs Position of the tag Leg 18 13 72% Neck 19 13 68% Number of parents tagged One 19 15 79% Both 18 11 61% Breeding stage Late incubation 20 13 65% Chick rearing 17 13 76% Control 23 17 74% The only significant predictor of breeding success in this study was the laying date (Chi square test, χ21 = 4.43, p = 0.035). Earlier laying birds had a higher chance of breeding successfully than later breeders (Fig. 5 ) because eggs laid early in the season were more likely to hatch (Chi square test, χ21 = 12.18, p < 0.001). However, laying date did not have any effect on chick survival after hatching (Chi square test, χ21 = 0.09, p = 0.77). Nonetheless, laying date did not impact the PIT-tagging results as PIT tag treatments were randomly assigned. Out of the 38 birds we monitored with automatic RFID readers, 37 birds were successfully detected one week to one month after being tagged. One individual wasn’t detected due to a failure of the reader. Colony attendance, detection probability Attendance patterns were highly variable, the timings of the first detection were relatively homogeneously distributed during the whole night contrary to the timing of the last detection (Fig. 6 ). The time between the first and last detection in the same night varied among individuals from 32 s to 6 h 3 min (mean: 2 h 47 min). The number of detections per night varied between 1 and 33 (mean: 6.65). Individuals with neck implants were detected a higher number of times per night than individuals with leg bands (Chi square test, χ21 = 6.99, p = 0.008) (Fig. 7 B) throughout the season (Chi square test, χ21 = 0.80, p = 0.37). The timing of the first detection every night did not depend on the position of the tag (Chi square test, χ21 = 3.21, p = 0.07) (Fig. 7 A) and was also consistent through the season (Chi square test, χ21 = 0.16, p = 0.69). The timing of the last detection every night did not depend on the position of the tag (Chi square test, χ21 = 1.14, p = 0.28) but tended to increase as the breeding season progresses (Chi square test, χ21 = 6.20, p = 0.012). We considered two variables for the CMR analysis: the group g (two different positions of marking) and the time t . We started with the most general model ϕ(g*t)p(g*t) and ended up with the model ϕ(.)p(g) being the most parsimonious (Table 3 ). There was no significant difference in detection probability between individuals marked on the leg (p = 0.832, 95% CI : [0.752,0.891]) or subcutaneously in the neck (p = 0.942, 95% CI : [0.854,0.979]). Survival chances were close to one (ϕ = 0.993, 95% CI : [0.956,0.999]). Table 3 Summary of model selection analysis of Rhinoceros auklet survival (ϕ) and resighting probability (p) depending on the position of their tag (g) and the day(t), c = 1 stands for survival probability constrained to be equal 1, ω is the weight of a particular model (relative support in the data) Model AICc ΔAICc ω Nb. Parameter Deviance 1 ϕ(.)p(g) 151.02 0 0,81 3 82.94 2 ϕ(.)p(.) 154.06 3,04 0,18 2 88,05 3 ϕ(.)p(g*t) 159,99 8,97 0 13 69,61 4 ϕ(c = 1)p(g) 165,33 14,32 0 2 99,33 5 ϕ(g*t)p(g*t) 177,45 26,43 0 22 64,29 DISCUSSION We used an experimental approach to determine the effects of PIT tagging on rhinoceros auklet breeding outcomes. Our approach will permit the development of a broader scale rhinoceros auklet automatic detection network on Middleton Island to record nest attendance and adult survival in future years. Our results suggest that the effects of PIT tagging on breeding success are negligible. Specifically, a power analysis shows that given our effect sizes, we would need 2 000 000 individuals to detect a statistically-significant (P < 0.05) difference between control and PIT tagged, 1858 individuals to detect a difference between incubation and chick-rearing and 424 individuals to detect a difference between single and double tagged. In short, the effects would only be measurable statistically with enormous sample sizes. Parental commitment towards breeding increases as the breeding season progresses. Thus, we expected that PIT tagging during incubation would cause higher abandonment than during chick rearing. This effect has been documented on rhinoceros auklets (Sun et al. 2020 ) as well as other burrowing seabird species (Carey 2009 ), although Kelly et al. ( 2015 ) found no impact of disturbance during incubation on breeding success of Atlantic puffins. However, we did not detect a difference in abandonment between breeding stages. This result most likely reflects the high effort we exerted in reducing disturbance as much as possible. Artificial nest boxes were particularly useful for that purpose, as the birds were easily accessible. The handling time was only three to five minutes long. We did not observe rhinoceros auklets displaying signs of high stress (e.g., breathing heavily, trying to escape) during the marking process. In addition, and unlike most monitoring tools, PIT tags are extremely small and lightweight. The PIT tags we used weighted ≈ 0.1g which represents around 0.02% of the birds’ mass. Our results are encouraging as both tagging and handling have well documented negative effect on seabird reproductive success (Rodway et al. 1996 ; Whidden et al. 2007 ), including reduced colony attendance (Söhle et al. 2000 ), chick growth rate (Ackerman et al. 2010 ; Villard et al. 2011 ) and higher nest abandonment (Sun et al. 2020 ). Considering our results, we can make recommendations for future PIT tagging experiments on rhinoceros auklets, and likely other burrow-nesting birds. Individuals should be marked during the last days of incubation or the very first days of chick rearing when they are accessible during daytime. Tagging individuals at night requires many visits to the same burrows multiple times, which can disturb individuals in the colony. However, this should be considered with precaution as handling seabirds during incubation goes against most recommendations (e.g. Elliott et al. 2010 ; Elliott 2016 ; Sun et al. 2020 ). As neither the number of adults tagged, nor the position of the tag seem to have any effect on reproductive success, we believe both adults of every burrow should be tagged in the neck. Having both adults tagged is an opportunity to study nest attendance at a finer scale, while neck implants are better fitted for the detection technology we used and reduce risks of tag loss. Indeed, the PIT tag need to be in a particular orientation when going through the antenna to maximize detection probability. Depending on the size of the access tunnel or individual walking physiology, the bird’s leg might not have the right orientation. PIT tags oriented perpendicularly to the magnetic field induced by the antenna would have a low detection probability, which could end up in data loss. This could be the reason why individuals with neck implants are detected a higher number of times each night. This could also be attributed to a difference in individual behavior but our data don't allow us to determine this. During the next season, several burrows will be monitored constantly with infrared cameras which will help us understand that phenomenon better. Lastly, detecting the PIT tag with a handheld detector through the opening atop the nest box would be much simpler when implanted in the back than attached on the leg. Studies report various loss rates for subcutaneously implanted pit tags. The size of the bird and the injection method seem to be important factors (Bonter and Bridge 2011 ). However, the tag loss rate was 0% on our sample (n = 38). In addition, for diving species, subcutaneous tagging might help decrease the added drag, as internal implantation of tags generally causes reduced impacts (Wilson et al. 1986 ; White et al. 2013 ; Evans et al. 2020 ). For example, positioning tags on the leg or the tail can cause instability (Vandenabeele et al. 2014 ; Elliott 2016 ). A study on crested auklets ( Aethia cristatella ) showed that a tarsus mounted tracking device (1% of the bird body mass) changed the behavior and at sea survival of marked individuals (Robinson and Jones 2014 ). Similarly, increasing buoyancy or mass via a leg-mounted tag altered the dive behaviour of thick-billed murres ( Uria lomvia ; Elliott et al. 2007 ), and attaching a leg-mounted tag for a year increased stress (corticosterone) in the same species (Elliott et al. 2012 ). The mass of the 3D-printed leg band and PIT tag we used in our study was around 1g (≈ 0.2% of the body mass), yet it could still have undesirable effects that we can avoid with subcutaneous implants. However, this statement has to be taken cautiously as all tags should be considered to have an impact even if they are hard to detect (Elliott 2016 ). The impact of such small devices might be particularly hard to detect as their mass are negligible. They could still have some long-term negative impact on survival (some marked individuals could suffer lesions from the tag migrating in the body) or may affect reproduction during subsequent years. For this reason, it is important to carry this study during several years before concluding on potential PIT tagging effects. Nonetheless, PIT tagging reduces disturbance on birds compared to manual burrow checks and GPS tagging due to decreased human presence on colonies. Thus, combining PIT tagging and automatic detection devices is a valuable method in studying sensitive seabird species during their breeding season. Several detectors revealed individuals visiting alternate burrows in our study. This behavior has been observed in Leach’s storm-petrel (Zangmeister et al. 2009 ) but not in the rhinoceros auklet. This phenomenon is unlikely to be due to a bird seeking for extra pair copulation, as data were collected late in the breeding season. One possibility is that those extra burrow visits could be attempts at kleptoparasitism (Senzaki et al. 2014 ). Monitoring intra-specific kleptoparasitic behaviors could be a way to monitor ecosystem health via food shortages. Indeed, this behavior is most likely to happen when food availability is scarce (Beintema 1997 ; Ashbrook et al. 2008 ). This experiment also revealed that parents could come back to a burrow even after the chick disappeared. During productivity checks, we found several burrows without a chick that had one before. We considered the absence of a chick as proof of nest abandonment by the parents, yet no corpse was found in the burrow. In two cases, the parents came back to the nest after we concluded the burrow was abandoned. In one case, both parents had a nest attendance pattern similar to successfully breeding birds even if the chick was considered dead two weeks previously. Clearly, auklets continue visit their burrows even after chicks are dead. These observations highlight the potential of PIT tagging to bring more knowledge on certain species. There is growing evidence that, even if monitoring seabird species gives us access to helpful data in understanding their biology and the state of their environment, monitoring is done at the expense of their fitness. This problem is concerning, especially during long studies that could have negative long-term carryover effects on populations. In extreme cases, researchers could be missing important factors that would be otherwise demonstrated in an undisturbed population. PIT tagging could be used extensively in sensitive seabird species and in the light of our results and previous ones, should be considered for rhinoceros auklets, other puffins and other burrow-nesting species. In conclusion, PIT tagging rhinoceros auklets nesting in artificial burrows is a promising way to monitor their behavior, breeding outcomes and long-term survival while having the least possible disturbance. This technique could be applied to other sensitive seabird species with a similar biology like tufted puffins ( Fratercula cirrhata ). By replacing usual nest monitoring with automatic PIT tag recording, we reduce disturbance and probability of burrow collapse due to less frequent visits. Declarations Acknowledgements We thank David Jadhon, Stella Solasz, Gabrielle Denis and Haley Gee for assistance with field work. Funding The research was funded by the Natural Sciences & Engineering Research Council of Canada, GulfWatch Alaska and Environment & Climate Change Canada. Competing Interests The authors have no relevant financial or non-financial interests to disclose Authors Contributions Leo Marcouillier, Shannon Whelan, Kyle H. Elliott contributed to the study conception and design. The detectors that made this study possible were built by Dave Fifield. Material preparation and data collection were performed by Leo Marcouillier, Elliane Miranda, Shannon Whelan and Chinatsu Nakajima. Analysis were performed by Leo Marcouillier. The first draft of this manuscript was written by Leo Marcouillier and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript Data Availability The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request. Ethics approval All activities were approved by the McGill Animal Use Protocol 2016-7814 and via permits from the US Fish & Wildlife Service and the Alaska Department of Fish & Game. Authors and affiliations Leo Marcouillier 1 , Eliane Miranda 1 , Shannon Whelan 1 , Dave Fifield 2 , Scott Hatch 3 , Akiko Shoji 4 , Chinatsu Nakajima 4 and Kyle H. 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J Field Ornithol 57:295–299 Zangmeister J, Haussmann M, Cerchiara P, Jack, Mauck R (2009) Incubation failure and nest abandonment by Leach’s Storm-Petrels detected using PIT tags and temperature loggers. J Field Ornithol 80:373–379. https://doi.org/10.1111/j.1557-9263.2009.00243.x Supplementary Files AppendixA.pdf Cite Share Download PDF Status: Published Journal Publication published 22 Feb, 2024 Read the published version in Marine Biology → Version 1 posted Editorial decision: Revise and Resubmit 13 Aug, 2023 Reviewers agreed at journal 22 Jul, 2023 Reviewers invited by journal 07 Jul, 2023 Editor assigned by journal 06 Jul, 2023 First submitted to journal 26 Jun, 2023 You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. 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Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-3112880","acceptedTermsAndConditions":true,"allowDirectSubmit":false,"archivedVersions":[],"articleType":"Research Article","associatedPublications":[],"authors":[{"id":216744796,"identity":"75bf9fd4-b485-4c5c-bf51-519eed38d3e3","order_by":0,"name":"Léo Marcouillier","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAABCElEQVRIiWNgGAWjYBACPgSTsfHAAwMGBn4QO6EAtxY2JC0NBxKAWiQbQFoMiNLCwHAgAUgYHAAx8Wlhbz7AdKPmnjy/RDLQlgKbfOPzqxM/AF0ozy92ALsWnmMJzDnHig1nzkgEOSzNctuNt5slgA4znDk7AbsWiRwD5hy2hASDG2Athw3MbpzdANKSYHAbhxb5N0At/+Ba/hsYzzi7+QdeLRI8Bsy5bXAtBwwM+Hu34beFJy3hcG5fguHMnocgLckGEjd4t1kkGEjg9As/++GDj3O+Jcjzs6c/fPDhj50Bf//ZzTd/VNjI80tj1wICB1C5EmCVEjiVY7P4AEElo2AUjIJRMLIAAMNlYDG9seaYAAAAAElFTkSuQmCC","orcid":"https://orcid.org/0009-0009-0865-0589","institution":"McGill University Department of Natural Resource Sciences","correspondingAuthor":true,"prefix":"","firstName":"Léo","middleName":"","lastName":"Marcouillier","suffix":""},{"id":216744797,"identity":"2de40d71-903a-4cca-bb8f-64e0298d43f0","order_by":1,"name":"Eliane Miranda","email":"","orcid":"","institution":"McGill University Department of Natural Resource Sciences","correspondingAuthor":false,"prefix":"","firstName":"Eliane","middleName":"","lastName":"Miranda","suffix":""},{"id":216744798,"identity":"e99201df-b4c1-42c5-bb1b-36cba4c36e61","order_by":2,"name":"Shannon Whelan","email":"","orcid":"","institution":"McGill University Department of Natural Resource Sciences","correspondingAuthor":false,"prefix":"","firstName":"Shannon","middleName":"","lastName":"Whelan","suffix":""},{"id":216744799,"identity":"6eb815e0-80d1-46e6-ac50-66deba525714","order_by":3,"name":"Dave Fifield","email":"","orcid":"","institution":"Environment and Climate Change Canada","correspondingAuthor":false,"prefix":"","firstName":"Dave","middleName":"","lastName":"Fifield","suffix":""},{"id":216744800,"identity":"896faf51-f146-4379-af4b-6c41415b15ee","order_by":4,"name":"Scott Hatch","email":"","orcid":"","institution":"Institute for Seabird Research and Conservation","correspondingAuthor":false,"prefix":"","firstName":"Scott","middleName":"","lastName":"Hatch","suffix":""},{"id":216744801,"identity":"abfdd693-fda6-4dc2-8849-335cec903219","order_by":5,"name":"Akiko Shoji","email":"","orcid":"","institution":"University of Tsukuba Graduate School of Life and Environmental Sciences: Tsukuba Daigaku Daigakuin Seimei Kankyo Kagaku Kenkyuka","correspondingAuthor":false,"prefix":"","firstName":"Akiko","middleName":"","lastName":"Shoji","suffix":""},{"id":216744802,"identity":"636424f5-0864-498c-8b5a-a3aca85b413f","order_by":6,"name":"Chinatsu Nakajima","email":"","orcid":"","institution":"University of Tsukuba Graduate School of Life and Environmental Sciences: Tsukuba Daigaku Daigakuin Seimei Kankyo Kagaku Kenkyuka","correspondingAuthor":false,"prefix":"","firstName":"Chinatsu","middleName":"","lastName":"Nakajima","suffix":""},{"id":216744803,"identity":"45af5365-66c2-47f3-8415-b19ba5de6a50","order_by":7,"name":"Kyle Elliott","email":"","orcid":"","institution":"McGill University Department of Natural Resource Sciences","correspondingAuthor":false,"prefix":"","firstName":"Kyle","middleName":"","lastName":"Elliott","suffix":""}],"badges":[],"createdAt":"2023-06-27 01:00:03","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-3112880/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-3112880/v1","draftVersion":[],"editorialEvents":[{"content":"https://doi.org/10.1007/s00227-023-04387-x","type":"published","date":"2024-02-22T15:01:20+00:00"}],"editorialNote":"","failedWorkflow":false,"files":[{"id":39924753,"identity":"e341b063-208a-4d20-8981-1e08bbb471f5","added_by":"auto","created_at":"2023-07-12 14:51:02","extension":"png","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":463591,"visible":true,"origin":"","legend":"\u003cp\u003eDesign of the artificial burrows used in this study\u003c/p\u003e","description":"","filename":"1.png","url":"https://assets-eu.researchsquare.com/files/rs-3112880/v1/ff7413a7302d58613846257c.png"},{"id":39924750,"identity":"4a39ef06-825f-458b-b7b4-ba0f5a600576","added_by":"auto","created_at":"2023-07-12 14:51:02","extension":"png","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":700672,"visible":true,"origin":"","legend":"\u003cp\u003eRhinoceros auklet equipped with a leg band (left). Marking a rhinoceros auklet with a subcutaneous implant in the neck (right)\u003c/p\u003e","description":"","filename":"2.png","url":"https://assets-eu.researchsquare.com/files/rs-3112880/v1/f7e9c95a9a5dbe2b9d77b221.png"},{"id":39924754,"identity":"9745182e-7de6-4589-8627-c54b93b5f0db","added_by":"auto","created_at":"2023-07-12 14:51:02","extension":"png","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":141903,"visible":true,"origin":"","legend":"\u003cp\u003eAutomatic Passive Integrated Transponder (PIT) tag reader installed in a rhinoceros auklet artificial burrow. The antenna is placed as parallel as possible to the entrance tunnel to reduce disturbance and to prevent the birds from dragging into the burrow.\u003c/p\u003e","description":"","filename":"3.png","url":"https://assets-eu.researchsquare.com/files/rs-3112880/v1/e8d04ad69f0012a252aed003.png"},{"id":39924751,"identity":"8a483860-e5fa-4c4e-ab69-af68b1b8e6ac","added_by":"auto","created_at":"2023-07-12 14:51:02","extension":"png","order_by":4,"title":"Figure 4","display":"","copyAsset":false,"role":"figure","size":8331,"visible":true,"origin":"","legend":"\u003cp\u003eProbability of a successful breeding ± S.E between different tag positions\u003c/p\u003e","description":"","filename":"4.png","url":"https://assets-eu.researchsquare.com/files/rs-3112880/v1/b1750f42fe21d7a0574ba510.png"},{"id":39924755,"identity":"41b0bb69-9839-4499-9458-1ea9d9b77edb","added_by":"auto","created_at":"2023-07-12 14:51:02","extension":"png","order_by":5,"title":"Figure 5","display":"","copyAsset":false,"role":"figure","size":9116,"visible":true,"origin":"","legend":"\u003cp\u003eInfluence of laying date on breeding success\u003c/p\u003e","description":"","filename":"5.png","url":"https://assets-eu.researchsquare.com/files/rs-3112880/v1/dadd1ff1d7619e754590752e.png"},{"id":39924752,"identity":"db639f46-2238-49e3-bc68-1b4504e90b0f","added_by":"auto","created_at":"2023-07-12 14:51:02","extension":"png","order_by":6,"title":"Figure 6","display":"","copyAsset":false,"role":"figure","size":7151,"visible":true,"origin":"","legend":"\u003cp\u003eFrequency distribution of the rhinoceros auklets timing of first and last detection every night\u003c/p\u003e","description":"","filename":"6.png","url":"https://assets-eu.researchsquare.com/files/rs-3112880/v1/9abff852854d6c5481ac5b0d.png"},{"id":39924757,"identity":"99d2d4ef-eb2f-4c66-81be-e26bf1e568eb","added_by":"auto","created_at":"2023-07-12 14:51:02","extension":"png","order_by":7,"title":"Figure 7","display":"","copyAsset":false,"role":"figure","size":8610,"visible":true,"origin":"","legend":"\u003cp\u003eDifferences in colony attendance pattern depending on the PIT tag position\u003c/p\u003e","description":"","filename":"7.png","url":"https://assets-eu.researchsquare.com/files/rs-3112880/v1/80ff2f9d6d36bec165244ff3.png"},{"id":51648317,"identity":"8f5f0a1e-4bd6-4bcc-9c20-3f2e3d60498e","added_by":"auto","created_at":"2024-02-26 15:12:18","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":2168278,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-3112880/v1/7d2263a6-9e92-434a-a20a-392e9116e4cc.pdf"},{"id":39925749,"identity":"acd63ae2-6baf-4ade-a7b9-d490075a0ab3","added_by":"auto","created_at":"2023-07-12 14:59:02","extension":"pdf","order_by":4,"title":"","display":"","copyAsset":false,"role":"supplement","size":88765,"visible":true,"origin":"","legend":"","description":"","filename":"AppendixA.pdf","url":"https://assets-eu.researchsquare.com/files/rs-3112880/v1/1121547b54a2b2f394e0fac0.pdf"}],"financialInterests":"","formattedTitle":"PIT tagging does not measurably reduce reproductive success in sensitive burrow-nesting seabirds","fulltext":[{"header":"INTRODUCTION","content":"\u003cp\u003eThe uncertainty principle in field ecology states that an investigator will always disturb the behavior of the biological model they are studying (Lenington \u003cspan citationid=\"CR31\" class=\"CitationRef\"\u003e1979\u003c/span\u003e). Investigator disturbance and its consequences are widely studied in field ecology (Hockin et al. \u003cspan citationid=\"CR24\" class=\"CitationRef\"\u003e1992\u003c/span\u003e; De Jong and Hoback \u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e2006\u003c/span\u003e; Carey \u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e2009\u003c/span\u003e). For example, observing avian behavior via biologging can induce higher mortality and nest predation (Ib\u0026aacute;\u0026ntilde;ez-\u0026Aacute;lamo et al. \u003cspan citationid=\"CR26\" class=\"CitationRef\"\u003e2012\u003c/span\u003e), reduced breeding success (Sandvik and Barrett \u003cspan citationid=\"CR37\" class=\"CitationRef\"\u003e2001\u003c/span\u003e; Blackmer et al. \u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e2004\u003c/span\u003e) or abnormal behaviors (Brown and Morris \u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e1995\u003c/span\u003e; Burger \u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e1998\u003c/span\u003e). While these effects do not always interfere with the traits of interest (e.g., morphology), investigator disturbance can clearly bias estimates of important life history traits.\u003c/p\u003e \u003cp\u003eUsing Radio Frequency Identification (RFID) presents a potential solution to reduce disturbance on monitored seabirds while measuring patterns of nest attendance behavior (Tyson \u003cspan citationid=\"CR43\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). Individuals can be equipped with Passive Integrated Transponders (PIT) tags that are small and can be attached quickly without, for example, soiling feathers. It allows for the identification of marked individuals, improving resighting data collection through automated networks without the need for recapture for band-reading (Gibbons and Andrews \u003cspan citationid=\"CR19\" class=\"CitationRef\"\u003e2004\u003c/span\u003e; Bonter and Bridge \u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e2011\u003c/span\u003e). The technology is used on a variety of taxa and increases the general knowledge on population dynamics of multiple species by providing strong estimates of survival and recruitment rates (Rebke et al. \u003cspan citationid=\"CR34\" class=\"CitationRef\"\u003e2010\u003c/span\u003e; Sutherland and Dann \u003cspan citationid=\"CR41\" class=\"CitationRef\"\u003e2012\u003c/span\u003e; Horswill et al. \u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e2014\u003c/span\u003e). These demographic parameters can inform predictive models to fine-tune conservation plans depending on the different constraints a population is facing (Weller et al. \u003cspan citationid=\"CR47\" class=\"CitationRef\"\u003e2014\u003c/span\u003e).\u003c/p\u003e \u003cp\u003ePuffins (\u003cem\u003eFratercula\u003c/em\u003e and \u003cem\u003eCerorhinca spp.)\u003c/em\u003e, show strong responses to their environment through breeding success and foraging behaviour (Bost and Le Maho \u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e1993\u003c/span\u003e; Gjerdrum et al. \u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e2003\u003c/span\u003e; Sydeman et al. \u003cspan citationid=\"CR42\" class=\"CitationRef\"\u003e2017\u003c/span\u003e). However, puffins and other burrow-nesting auks are notably hard to study because of their high sensitivity to human disturbance (Rodway et al. \u003cspan citationid=\"CR36\" class=\"CitationRef\"\u003e1996\u003c/span\u003e; Whidden et al. \u003cspan citationid=\"CR48\" class=\"CitationRef\"\u003e2007\u003c/span\u003e; Elliott et al. \u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e2010\u003c/span\u003e; Harris and Wanless \u003cspan citationid=\"CR22\" class=\"CitationRef\"\u003e2011\u003c/span\u003e; Sun et al. \u003cspan citationid=\"CR40\" class=\"CitationRef\"\u003e2020\u003c/span\u003e; but see Kelly et al. \u003cspan citationid=\"CR28\" class=\"CitationRef\"\u003e2015\u003c/span\u003e). Rhinoceros auklets (\u003cem\u003eCerorhinca monocerata\u003c/em\u003e) are burrow nesting puffins that are mostly active on their colonies at night. Nocturnality makes the collection of observational data challenging, as color bands cannot be easily read from a distance, resulting in knowledge gaps for the species ecology. Rhinoceros auklets exhibit breeding site fidelity (Kubo et al. \u003cspan citationid=\"CR29\" class=\"CitationRef\"\u003e2018\u003c/span\u003e) making them a good target for long-term monitoring. However, executing such studies requires accessing burrows regularly, accelerating habitat destruction (Priddel and Carlile \u003cspan citationid=\"CR33\" class=\"CitationRef\"\u003e1995\u003c/span\u003e). Such practices can have strong deleterious effects on the long term (Wilson \u003cspan citationid=\"CR52\" class=\"CitationRef\"\u003e1986\u003c/span\u003e), increasing the risk of burrow collapsing as well as reducing their breeding success through higher nest abandonment rates.\u003c/p\u003e \u003cp\u003eGiven the sensitivity of some burrow-nesting seabirds, especially puffins, to human impacts (Watson et al. \u003cspan citationid=\"CR46\" class=\"CitationRef\"\u003e2014\u003c/span\u003e; Sun et al. \u003cspan citationid=\"CR40\" class=\"CitationRef\"\u003e2020\u003c/span\u003e), our objective was to set up a minimally invasive protocol for the long-term monitoring of rhinoceros auklets on Middleton Island, Alaska, through automatic Radio Frequency Identification (RFID).\u003c/p\u003e \u003cp\u003eWe used an experimental approach to test the effects of different PIT tagging protocols on nest abandonment probability by tagging birds (i) at different times of the breeding season (late incubation vs early chick rearing), (ii) externally and internally (subcutaneous implantation in the neck vs external attachment on a 3D-printed leg band) and (iii) at different intensities (single vs both adults in burrow tagged). We detected individuals using automatic RFID readers. We were particularly interested in whether breeding stage impacted abandonment rates, as some studies (Sun et al. \u003cspan citationid=\"CR40\" class=\"CitationRef\"\u003e2020\u003c/span\u003e) but not others (Kelly et al. \u003cspan citationid=\"CR28\" class=\"CitationRef\"\u003e2015\u003c/span\u003e) have documented increased abandonment during incubation, when adults are presumably less invested in their offspring because their subsequent survival is lower (i.e. chicks necessarily are more likely to survive to fledging than eggs). We were also interested in whether leg-mounted or internally implanted PIT tags would cause less abandonment, as leg-mounted devices can alter flying and diving behavior due to imbalanced distribution of weight and buoyance but implanted tags may cause infection (Hatch et al. \u003cspan citationid=\"CR23\" class=\"CitationRef\"\u003e2000\u003c/span\u003e; Elliott et al. \u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e2007\u003c/span\u003e; Vandenabeele et al. \u003cspan citationid=\"CR44\" class=\"CitationRef\"\u003e2014\u003c/span\u003e). This method provided an opportunity to learn more about cryptic nest attendance behavior.\u003c/p\u003e"},{"header":"METHODS","content":"\u003cdiv id=\"Sec3\" class=\"Section2\"\u003e \u003ch2\u003eStudy system\u003c/h2\u003e \u003cp\u003eWe collected data from rhinoceros auklets breeding in a colony on Middleton Island, Alaska (59.42\u0026deg; N, 146.32\u0026deg; W). The colony has been monitored since 1977 and diet and population metrics are collected annually since 1993. During the breeding season (April to August), this population of rhinoceros auklets nest in burrows dug in soil slopes dominated by salmonberry bushes (\u003cem\u003eRubea spectabilis\u003c/em\u003e). Nest attendance patterns and sensitivity to human disturbance differ between incubation and chick-rearing (Sun et al. \u003cspan citationid=\"CR40\" class=\"CitationRef\"\u003e2020\u003c/span\u003e). Parents are more likely to abandon the nest after human disturbance in the early stages of breeding. Breeding pairs lay a single egg in late April to early May and incubate for approximately 45 days. During incubation (and the first days of chick rearing), the parents typically take turns incubating the egg (or hatchling) for two days shifts. Parents will then both cease daytime burrow attendance and spend the daytime foraging at sea, returning to the colony once each night to feed the chick by delivering a \u0026ldquo;bill load\u0026rdquo;. These deliveries tend to include multiple prey items (usually fish) carried between the mandibles and dropped inside the nest chamber of the burrow (Gaston and Dechesne \u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e1996\u003c/span\u003e; Davoren and Burger \u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e1999\u003c/span\u003e; Kato et al. \u003cspan citationid=\"CR27\" class=\"CitationRef\"\u003e2003\u003c/span\u003e; Cunningham et al. \u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e2018\u003c/span\u003e). This phase lasts around 50 days until the chick fledges and leaves the nest (Harfenist and Ydenberg \u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e1995\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eWe conducted this study using artificial nest boxes. Between 2017 and 2021, 121 artificial nest boxes were installed in a limited area within a breeding colony of rhinoceros auklets on Middleton Island. The artificial burrows consist of two parts: A L-shaped wooden box made in \u0026frac12;-inch-thick plywood treated with wood preservative and a corrugated plastic tubing as entrance tunnel (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e). The top of the box is equipped with a trap door for easy access to the nesting chamber. The nest box floor is made of wire mesh. The nest box is buried in the ground, partially filled with soil, and then marked with a uniquely numbered stake to be easily re-located.\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec4\" class=\"Section2\"\u003e \u003ch2\u003eReproductive success monitoring\u003c/h2\u003e \u003cp\u003eWe checked nest boxes for the first time in 2022 on 20 May. We examined the boxes for the presence of an adult with an egg and floated eggs to estimate laying date (see below). We visited occupied nest boxes on May 30 and every 5 days thereafter until hatch to monitor breeding parameters (incl. hatching success, hatching date, chick survival and growth). At each visit, we recorded presence or absence of an adult and the temperature of the egg (cold or warm, indicative of how recently an adult was incubating). We measured chick weight (g) and wing chord (mm) 5 and 20 days after they were first found. Chicks were not disturbed between these checks.\u003c/p\u003e \u003cp\u003eA breeding attempt at a nest box was considered successful (breeding success\u0026thinsp;=\u0026thinsp;1) if the chick fledged. We checked for the presence of a live chick every 5 days, 45 days after the chick was first recorded as hatched. A chick was considered a successful fledgling if it was absent from the burrow during one of those post-45 day checks. The breeding attempt was considered unsuccessful (breeding success\u0026thinsp;=\u0026thinsp;0) if the egg was found cold on three consecutive checks, or the chick was found dead or missing before the second measurement (no chick was found dead after 45 days). Most failure resulted from the parents abandoning the nest. When a nest box was checked, the entrance was plugged to prevent the adult from escaping and potentially abandoning the nest. The lid of the nest box was cracked open to see its contents. If necessary, we checked manually for the presence and temperature of a chick or an egg.\u003c/p\u003e \u003cp\u003eDuring productivity checks, birds in nest boxes which had potentially been PIT-tagged before (see \u0026ldquo;PIT-tagging\u0026rdquo;) were read using a handheld \u003cem\u003ereader (RT100V8, RealTrace, ATRIA Trading SA, Le Parray en Yvelines, France)\u003c/em\u003e. If the bird showed signs of stress, we tried to feel its metal band instead to limit disturbance and abandonment risks. For similar reasons, we skipped nest boxes on productivity check days if one of the birds inhabiting the box had been tagged less than three days prior.\u003c/p\u003e \u003cp\u003eFloating height and angle are good predictors of the laying date (Liebezeit et al. \u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e2007\u003c/span\u003e). To estimate laying phenology, we used the flotation technique described in Sun et al. (\u003cspan citationid=\"CR40\" class=\"CitationRef\"\u003e2020\u003c/span\u003e) for rhinoceros auklets at our study site by measuring either the angle that eggs rested (sinking eggs) or the height of exposed egg above water (floating eggs).\u003c/p\u003e \u003cp\u003eFor a sinking egg, we used the equation:\u003cdiv id=\"Equa\" class=\"Equation\"\u003e\u003cdiv format=\"TEX\" class=\"mathdisplay\" id=\"FileID_Equa\" name=\"EquationSource\"\u003e\n$$\\begin{array}{c}Days until hatch=46-\\left(0.002*floating angl{e}^{2}+0.078*floating angle+1.16\\right) \\#\\left(1\\right)\\end{array}$$\u003c/div\u003e\u003c/div\u003e\u003c/p\u003e \u003cp\u003eFor a floating egg:\u003cdiv id=\"Equb\" class=\"Equation\"\u003e\u003cdiv format=\"TEX\" class=\"mathdisplay\" id=\"FileID_Equb\" name=\"EquationSource\"\u003e\n$$\\begin{array}{c}Days until hatch=46-\\left(2.014*floating height+20.027\\right) \\#\\left(2\\right)\\end{array}$$\u003c/div\u003e\u003c/div\u003e\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec5\" class=\"Section2\"\u003e \u003ch2\u003ePIT tagging\u003c/h2\u003e \u003cp\u003eWe found 63 occupied nest boxes on the first check. These nest boxes were assigned a treatment (Control, Late-incubation, or Chick-rearing). We assigned 20 nest boxes each to the Late-incubation and Chick-rearing groups: 10 boxes with a single adult tagged and 10 boxes with both adults tagged for a total of 60 birds with a PIT tag. Half of the birds were PIT-tagged subcutaneously in the neck and the other half were banded on one leg with a special plastic band 3D-printed to hold a PIT tag. The remaining 23 nest boxes were assigned to the control group. Treatment groups were assigned to be balanced across phenology and space. Tag position (neck or leg) and number of adults tagged per nest box (one or both) were assigned via a random number generator. Three nest boxes in the chick rearing treatment group were excluded because the egg never hatched. Burrows assigned to the Late-incubation treatment were tagged 10 days before the estimated date of hatching. Chick-rearing birds were tagged as soon as they were found with a chick. If a chick was found without a parent during a productivity check the nest box would be checked every night for one week until the parent was found. If an individual was marked less than three days before the next productivity check, its burrow was skipped during this check to reduce disturbance. In one burrow, an individual not found after one week of marking effort was excluded from the study.\u003c/p\u003e \u003cp\u003eBirds were marked with 12-mm EM4102 PIT tags (frequency\u0026thinsp;=\u0026thinsp;125kHz). The PIT tag was either placed in a 1.25-mm thick 3D-printed nylon leg band on the left leg, and secured with super glue and Tesa tape (tesa tape inc. 5825 Carnegie Boulevard, Charlotte, North Carolina 28209), or inserted in the lose neck skin between the scapulae (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003e).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003eA single-use needle was used for each bird. The PIT tag was sterilized in a chlorhexidine solution overnight and then stored in PBS solution until injection. The injection point was disinfected with a cotton ball soaked in 70% isopropyl solution to part the feathers. The same cotton ball was applied on the wound for several seconds after the injection to prevent the tag from falling out during the closing of the skin around the puncture wound. Tagged birds were also banded with metal U.S. Fish and Wildlife bands on the right leg. The first tagged bird in each nest box had a small piece of Tesa tape wrapped around the metal band. This facilitated rapid identification during productivity checks as well as the monitoring of tag failure rates (e.g., the PIT tag leg band would fall off or the implant would migrate in the body/not be detectable anymore).\u003c/p\u003e \u003cp\u003eWhen the bird was caught, its head was placed in a bag to reduce stress. The bird was released in the nest box from the tunnel immediately after being PIT tagged and the entrance was kept plugged for at least 5 minutes to prevent early abandonment. Capture and release time were recorded. Every late incubation bird (n\u0026thinsp;=\u0026thinsp;30) and 10 chick rearing birds were tagged in the morning between 09:00 and 13:00. The 15-remaining chick rearing birds were tagged at night between 23:00 and 04:00. Implanting a PIT tag in the neck took 6 min 44 s (SD: 2 min 33 s) attaching a leg band equipped with a PIT tag took 4 min 8 s (SD: 1 min 7 s)\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec6\" class=\"Section2\"\u003e \u003ch2\u003eAutomatic PIT tag reading\u003c/h2\u003e \u003cp\u003eLoggers used custom-built automated, low-powered PIT tag readers. The device is made of two parts. The first is a custom designed 9.5cm x 8cm circuit board that holds a microcontroller, an internal clock and the memory that stores the record of every PIT tag reading. The circuit board was secured in a pelican case with silica gel inside to protect it from humidity. The second part is the antenna which is made of a copper wire coiled around a 3D-printed flexible ring dipped in Plasti Dip (Plast Dip International, 3920 Pheasant Ridge Drive Blaine, MN 55449) and wrapped in electrical tape. The diameter of the antenna measures 130 mm which fits the internal diameter of the nest boxes\u0026rsquo; access tunnel. When powered, the antenna induces a magnetic field. To constrain its magnetic field frequency to the desired value of 125 kHz, the circuit board regularly reads the actual frequency of the magnetic field induced by the antenna and switches capacitors of appropriate value into the circuit to correct for frequency drift. When a PIT tag goes through the antenna, the magnetic field is disturbed which is detected by the circuit board, leading to a record. Each time the PIT tag is detected, its unique ID, the date and time are logged.\u003c/p\u003e \u003cp\u003eThe system was powered by a 12-V marine deep-cyle battery (model SCS225; Trojan Battery Company 12380 Clark Street Santa Fe Springs, CA 90670) connected to a battery charger connected to a 120-V power source, therefore allowing for complete autonomy the whole season. Power was distributed to multiple burrow monitors by a 16-position terminal block (OONO MD-D1349P-1, \u003cspan class=\"ExternalRef\"\u003e\u003cspan class=\"RefSource\"\u003ehttps://czh-labs.com/products/screw-mount-2x16-position-screw-terminal-block-power-distribution-module-1280\u003c/span\u003e\u003cspan address=\"https://czh-labs.com/products/screw-mount-2x16-position-screw-terminal-block-power-distribution-module-1280\" targettype=\"URL\" class=\"RefTarget\"\u003e\u003c/span\u003e\u003c/span\u003e). The power station was positioned at the entrance of the colony and was protected from the rain using plastic covering. The power station and the PIT tag readers were connected with 30-m cables allowing us to reach a major part of the colony. The readers were then spread in the colony and set up at the nest boxes (Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003e). The antennae were placed as parallel as possible to the access tunnel to reduce disturbance to individuals accessing the burrow and to maximize detection probability. We had 12 working readers. Every week, we changed the position of the reader to be able to monitor as many burrows as possible during the season. Every occupied burrow as well as 2 burrows where the chick disappeared from the nest were monitored with readers. This represented 27 boxes and 38 birds (15 tagged in the neck and 23 tagged on the leg).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec7\" class=\"Section2\"\u003e \u003ch2\u003eStatistical analyses\u003c/h2\u003e \u003cp\u003eAll statistical analyses were completed using R version 4.0.2 (R core team 2020). We tested the effect of different aspects of PIT tagging on abandonment with binomial generalized linear models using a chi squared significance test. All interactions were first considered unless specified. If the highest rank interaction term was not significant, it was removed until only significant interactions and/or single terms remained.\u003c/p\u003e \u003cp\u003eThe effect of PIT tag location, number of adults PIT tagged, and breeding stage on abandonment were tested on the subset of PIT tagged birds. We compared the breeding success of control and PIT tagged rhinoceros auklets depending on their breeding stage (incubation or chick rearing) with Fisher\u0026rsquo;s exact test. A statistical power analysis was then run on the three following comparisons: breeding success of PIT tagged vs control individuals, individuals marked on the leg vs subcutaneously and individuals marked during incubation vs chick rearing with the R package \u0026ldquo;pwr\u0026rdquo;. The effect of PIT tagging on chick daily wing growth and weight gain was tested with an ANOVA.\u003c/p\u003e \u003cp\u003eGiven the flotation technique is only accurate within about 10 days, we used the following estimate for hatching date:\u003cdiv id=\"Equc\" class=\"Equation\"\u003e\u003cdiv format=\"TEX\" class=\"mathdisplay\" id=\"FileID_Equc\" name=\"EquationSource\"\u003e\n$$\\begin{array}{c}Hatching date=\\frac{\\left(Date chick first seen\\right)-\\left(Date egg last seen\\right)}{2} \\#\\left(3\\right)\\end{array}$$\u003c/div\u003e\u003c/div\u003e\u003c/p\u003e \u003cp\u003eHowever, we kept the egg flotation estimate (1) or (2) when the egg didn\u0026rsquo;t hatch.\u003c/p\u003e \u003cp\u003eWe investigated differences in attendance pattern (number of detection.night\u003csup\u003e-1\u003c/sup\u003e, timing of the first and last detection) depending on the position of the tag and how advanced the breeding season was with linear models using a random effect on individual ID to control for inter-individual variation. When an individual was recorded only once during a particular day, this record was removed from the colony presence analysis.\u003c/p\u003e \u003cp\u003eTo determine whether the position of tagging influenced the detection probability, we ran a capture-mark-recapture (CMR) analysis on the subset of marked individuals. We used one week of capture history from 33 birds detected between 15 July and 7 August (example of detection record in appendix A). The analysis was completed in MARK version 9.x (White and Burnham \u003cspan citationid=\"CR50\" class=\"CitationRef\"\u003e1999\u003c/span\u003e). This was done via standard live encounter mark-recapture models (Lebreton et al. \u003cspan citationid=\"CR30\" class=\"CitationRef\"\u003e1992\u003c/span\u003e), where the probability of an individual being seen is defined by 2 parameters: the probability the animal survived and remained in the sample area (ϕ), and the probability that the animal was encountered (p), conditional on being alive and in the sample area. Following Lebreton et al. (\u003cspan citationid=\"CR30\" class=\"CitationRef\"\u003e1992\u003c/span\u003e) methods, we began with a general model and examined simpler alternatives. Model selection was based on Akaike\u0026rsquo;s Information Criterion (AIC). The model with lowest AIC being considered as the most parsimonious one. The parameters estimated from the best model are given with 95% confidence interval (95% CI) computed from the Hessian matrix.\u003c/p\u003e \u003c/div\u003e"},{"header":"RESULTS","content":"\u003cp\u003eIn total, 55 birds were PIT tagged in 37 different artificial burrows (Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e).\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab1\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 1\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eNumber of artificial burrows in each treatment group: Control (0 parent tagged), Single (1 parent tagged), Double (both parents tagged), depending on their breeding stage (Incubation vs Chick rearing)\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"3\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/th\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003eLate Incubation\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c3\"\u003e \u003cp\u003eChick Rearing\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eControl\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colspan=\"2\" nameend=\"c3\" namest=\"c2\"\u003e \u003cp\u003e23\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eSingle\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e10 (5 on leg, 5 in neck)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e9 (3 on leg, 6 in neck)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eDouble\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e10 (5 on leg, 5 in neck)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e8 (5 on leg, 3 in neck)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cp\u003eAmong the 63 boxes we monitored, 52 successfully hatched an egg (82%) and 43 of the chicks fledged, which made an overall breeding success of 68%. Some chicks were still present in the burrow for the last productivity check on 13 August 2022. These chicks (Age\u0026thinsp;\u0026plusmn;\u0026thinsp;SD\u0026thinsp;=\u0026thinsp;50\u0026thinsp;\u0026plusmn;\u0026thinsp;8 d, n\u0026thinsp;=\u0026thinsp;22) were considered as successful fledglings. This assumption is reasonable since the probability of not being fledged on the last check depended on the age of the chick (Chi square test, χ21\u0026thinsp;=\u0026thinsp;6.59, p\u0026thinsp;=\u0026thinsp;0.01) and not the treatment group (Chi square test, χ22\u0026thinsp;=\u0026thinsp;4.59, p\u0026thinsp;=\u0026thinsp;0.10). PIT tagging did not significantly influence egg hatching success (Chi square test, χ21\u0026thinsp;=\u0026thinsp;0.52, p\u0026thinsp;=\u0026thinsp;0.47) nor chick fledging (Chi square test, χ21\u0026thinsp;=\u0026thinsp;1.02, p\u0026thinsp;=\u0026thinsp;0.31). Overall, we observed similar breeding success of control birds and birds PIT tagged during incubation or chick rearing (Fisher\u0026rsquo;s exact test, all p\u0026thinsp;\u0026gt;\u0026thinsp;0.8). In addition, control individuals, as well as individuals tagged on the leg or in the neck had a similar breeding success (Fig.\u0026nbsp;\u003cspan refid=\"Fig4\" class=\"InternalRef\"\u003e4\u003c/span\u003e).\u003c/p\u003e \u003cp\u003ePIT tagging of adults also had little effect on chick development, daily wing growth (ANOVA, F(2,39)\u0026thinsp;=\u0026thinsp;2.69 p\u0026thinsp;=\u0026thinsp;0.0807) (Wing length.day\u003csup\u003e-1\u003c/sup\u003e \u0026plusmn; SD\u0026thinsp;=\u0026thinsp;Control group: 2.4\u0026thinsp;\u0026plusmn;\u0026thinsp;0.56 cm.day\u003csup\u003e-1\u003c/sup\u003e, n\u0026thinsp;=\u0026thinsp;16, one individual tagged: 2.9\u0026thinsp;\u0026plusmn;\u0026thinsp;0.62 cm.day\u003csup\u003e-1\u003c/sup\u003e, n\u0026thinsp;=\u0026thinsp;15, both individuals tagged: 2.4\u0026thinsp;\u0026plusmn;\u0026thinsp;0.75 cm.day\u003csup\u003e-1\u003c/sup\u003e, n\u0026thinsp;=\u0026thinsp;11) or weight gain (F(2,39)\u0026thinsp;=\u0026thinsp;0.38 p\u0026thinsp;=\u0026thinsp;0.69) (Mass.day\u003csup\u003e-1\u003c/sup\u003e \u0026plusmn; SD\u0026thinsp;=\u0026thinsp;Control group: 6.9\u0026thinsp;\u0026plusmn;\u0026thinsp;1.6 g.day\u003csup\u003e-1\u003c/sup\u003e, n\u0026thinsp;=\u0026thinsp;16, one individual tagged: 7.4\u0026thinsp;\u0026plusmn;\u0026thinsp;2.2 g.day\u003csup\u003e-1\u003c/sup\u003e, n\u0026thinsp;=\u0026thinsp;15, both individuals tagged: 7.2\u0026thinsp;\u0026plusmn;\u0026thinsp;1.6 g.day\u003csup\u003e-1\u003c/sup\u003e, n\u0026thinsp;=\u0026thinsp;11).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003eBreeding success was not related to PIT tagging on the subset of tagged birds (n\u0026thinsp;=\u0026thinsp;37 boxes). The position of tagging (leg or neck) (Chi square test, χ21\u0026thinsp;=\u0026thinsp;0.18, p\u0026thinsp;=\u0026thinsp;0.67), the number of birds tagged in the pair (Chi square test, χ21\u0026thinsp;=\u0026thinsp;1.49, p\u0026thinsp;=\u0026thinsp;0.22) and breeding stage (Chi square test, χ21\u0026thinsp;=\u0026thinsp;0.56, p\u0026thinsp;=\u0026thinsp;0.46) did not influence abandonment (Table\u0026nbsp;\u003cspan refid=\"Tab2\" class=\"InternalRef\"\u003e2\u003c/span\u003e).\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab2\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 2\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eProportion of pairs that successfully fledged an offspring for each group\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"5\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c5\" colnum=\"5\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/th\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003eTreatment\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c3\"\u003e \u003cp\u003en\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c4\"\u003e \u003cp\u003eNumber of successful pairs\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c5\"\u003e \u003cp\u003ePercentage of successful pairs\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003ePosition of the tag\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eLeg\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e18\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e13\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e72%\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eNeck\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e19\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e13\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e68%\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003eNumber of parents tagged\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eOne\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e19\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e15\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e79%\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eBoth\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e18\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e11\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e61%\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003eBreeding stage\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eLate incubation\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e20\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e13\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e65%\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eChick rearing\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e17\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e13\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e76%\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colspan=\"2\" nameend=\"c2\" namest=\"c1\"\u003e \u003cp\u003eControl\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e23\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e17\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e74%\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cp\u003eThe only significant predictor of breeding success in this study was the laying date (Chi square test, χ21\u0026thinsp;=\u0026thinsp;4.43, p\u0026thinsp;=\u0026thinsp;0.035). Earlier laying birds had a higher chance of breeding successfully than later breeders (Fig.\u0026nbsp;\u003cspan refid=\"Fig5\" class=\"InternalRef\"\u003e5\u003c/span\u003e) because eggs laid early in the season were more likely to hatch (Chi square test, χ21\u0026thinsp;=\u0026thinsp;12.18, p\u0026thinsp;\u0026lt;\u0026thinsp;0.001). However, laying date did not have any effect on chick survival after hatching (Chi square test, χ21\u0026thinsp;=\u0026thinsp;0.09, p\u0026thinsp;=\u0026thinsp;0.77). Nonetheless, laying date did not impact the PIT-tagging results as PIT tag treatments were randomly assigned.\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003eOut of the 38 birds we monitored with automatic RFID readers, 37 birds were successfully detected one week to one month after being tagged. One individual wasn\u0026rsquo;t detected due to a failure of the reader.\u003c/p\u003e \u003cdiv id=\"Sec9\" class=\"Section2\"\u003e \u003ch2\u003eColony attendance, detection probability\u003c/h2\u003e \u003cp\u003eAttendance patterns were highly variable, the timings of the first detection were relatively homogeneously distributed during the whole night contrary to the timing of the last detection (Fig.\u0026nbsp;\u003cspan refid=\"Fig6\" class=\"InternalRef\"\u003e6\u003c/span\u003e). The time between the first and last detection in the same night varied among individuals from 32 s to 6 h 3 min (mean: 2 h 47 min). The number of detections per night varied between 1 and 33 (mean: 6.65).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003eIndividuals with neck implants were detected a higher number of times per night than individuals with leg bands (Chi square test, χ21\u0026thinsp;=\u0026thinsp;6.99, p\u0026thinsp;=\u0026thinsp;0.008) (Fig.\u0026nbsp;\u003cspan refid=\"Fig7\" class=\"InternalRef\"\u003e7\u003c/span\u003eB) throughout the season (Chi square test, χ21\u0026thinsp;=\u0026thinsp;0.80, p\u0026thinsp;=\u0026thinsp;0.37). The timing of the first detection every night did not depend on the position of the tag (Chi square test, χ21\u0026thinsp;=\u0026thinsp;3.21, p\u0026thinsp;=\u0026thinsp;0.07) (Fig.\u0026nbsp;\u003cspan refid=\"Fig7\" class=\"InternalRef\"\u003e7\u003c/span\u003eA) and was also consistent through the season (Chi square test, χ21\u0026thinsp;=\u0026thinsp;0.16, p\u0026thinsp;=\u0026thinsp;0.69). The timing of the last detection every night did not depend on the position of the tag (Chi square test, χ21\u0026thinsp;=\u0026thinsp;1.14, p\u0026thinsp;=\u0026thinsp;0.28) but tended to increase as the breeding season progresses (Chi square test, χ21\u0026thinsp;=\u0026thinsp;6.20, p\u0026thinsp;=\u0026thinsp;0.012).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003eWe considered two variables for the CMR analysis: the group \u003cem\u003eg\u003c/em\u003e (two different positions of marking) and the time \u003cem\u003et\u003c/em\u003e. We started with the most general model ϕ(g*t)p(g*t) and ended up with the model ϕ(.)p(g) being the most parsimonious (Table\u0026nbsp;\u003cspan refid=\"Tab3\" class=\"InternalRef\"\u003e3\u003c/span\u003e). There was no significant difference in detection probability between individuals marked on the leg (p\u0026thinsp;=\u0026thinsp;0.832, 95% CI : [0.752,0.891]) or subcutaneously in the neck (p\u0026thinsp;=\u0026thinsp;0.942, 95% CI : [0.854,0.979]). Survival chances were close to one (ϕ\u0026thinsp;=\u0026thinsp;0.993, 95% CI : [0.956,0.999]).\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab3\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 3\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eSummary of model selection analysis of Rhinoceros auklet survival (ϕ) and resighting probability (p) depending on the position of their tag (g) and the day(t), c\u0026thinsp;=\u0026thinsp;1 stands for survival probability constrained to be equal 1, ω is the weight of a particular model (relative support in the data)\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"7\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c5\" colnum=\"5\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c6\" colnum=\"6\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c7\" colnum=\"7\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/th\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003eModel\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c3\"\u003e \u003cp\u003eAICc\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c4\"\u003e \u003cp\u003eΔAICc\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c5\"\u003e \u003cp\u003eω\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c6\"\u003e \u003cp\u003eNb. Parameter\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c7\"\u003e \u003cp\u003eDeviance\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eϕ(.)p(g)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e151.02\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e0\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e0,81\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e82.94\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eϕ(.)p(.)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e154.06\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e3,04\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e0,18\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e88,05\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eϕ(.)p(g*t)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e159,99\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e8,97\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e0\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e13\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e69,61\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eϕ(c\u0026thinsp;=\u0026thinsp;1)p(g)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e165,33\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e14,32\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e0\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e99,33\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e5\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eϕ(g*t)p(g*t)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e177,45\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e26,43\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e0\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e22\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e64,29\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003c/div\u003e"},{"header":"DISCUSSION","content":"\u003cp\u003eWe used an experimental approach to determine the effects of PIT tagging on rhinoceros auklet breeding outcomes. Our approach will permit the development of a broader scale rhinoceros auklet automatic detection network on Middleton Island to record nest attendance and adult survival in future years.\u003c/p\u003e \u003cp\u003eOur results suggest that the effects of PIT tagging on breeding success are negligible. Specifically, a power analysis shows that given our effect sizes, we would need 2 000 000 individuals to detect a statistically-significant (P\u0026thinsp;\u0026lt;\u0026thinsp;0.05) difference between control and PIT tagged, 1858 individuals to detect a difference between incubation and chick-rearing and 424 individuals to detect a difference between single and double tagged. In short, the effects would only be measurable statistically with enormous sample sizes.\u003c/p\u003e \u003cp\u003eParental commitment towards breeding increases as the breeding season progresses. Thus, we expected that PIT tagging during incubation would cause higher abandonment than during chick rearing. This effect has been documented on rhinoceros auklets (Sun et al. \u003cspan citationid=\"CR40\" class=\"CitationRef\"\u003e2020\u003c/span\u003e) as well as other burrowing seabird species (Carey \u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e2009\u003c/span\u003e), although Kelly et al. (\u003cspan citationid=\"CR28\" class=\"CitationRef\"\u003e2015\u003c/span\u003e) found no impact of disturbance during incubation on breeding success of Atlantic puffins. However, we did not detect a difference in abandonment between breeding stages. This result most likely reflects the high effort we exerted in reducing disturbance as much as possible. Artificial nest boxes were particularly useful for that purpose, as the birds were easily accessible. The handling time was only three to five minutes long. We did not observe rhinoceros auklets displaying signs of high stress (e.g., breathing heavily, trying to escape) during the marking process. In addition, and unlike most monitoring tools, PIT tags are extremely small and lightweight. The PIT tags we used weighted\u0026thinsp;\u0026asymp;\u0026thinsp;0.1g which represents around 0.02% of the birds\u0026rsquo; mass.\u003c/p\u003e \u003cp\u003eOur results are encouraging as both tagging and handling have well documented negative effect on seabird reproductive success (Rodway et al. \u003cspan citationid=\"CR36\" class=\"CitationRef\"\u003e1996\u003c/span\u003e; Whidden et al. \u003cspan citationid=\"CR48\" class=\"CitationRef\"\u003e2007\u003c/span\u003e), including reduced colony attendance (S\u0026ouml;hle et al. \u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e2000\u003c/span\u003e), chick growth rate (Ackerman et al. \u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e2010\u003c/span\u003e; Villard et al. \u003cspan citationid=\"CR45\" class=\"CitationRef\"\u003e2011\u003c/span\u003e) and higher nest abandonment (Sun et al. \u003cspan citationid=\"CR40\" class=\"CitationRef\"\u003e2020\u003c/span\u003e). Considering our results, we can make recommendations for future PIT tagging experiments on rhinoceros auklets, and likely other burrow-nesting birds. Individuals should be marked during the last days of incubation or the very first days of chick rearing when they are accessible during daytime. Tagging individuals at night requires many visits to the same burrows multiple times, which can disturb individuals in the colony. However, this should be considered with precaution as handling seabirds during incubation goes against most recommendations (e.g. Elliott et al. \u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e2010\u003c/span\u003e; Elliott \u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e2016\u003c/span\u003e; Sun et al. \u003cspan citationid=\"CR40\" class=\"CitationRef\"\u003e2020\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eAs neither the number of adults tagged, nor the position of the tag seem to have any effect on reproductive success, we believe both adults of every burrow should be tagged in the neck. Having both adults tagged is an opportunity to study nest attendance at a finer scale, while neck implants are better fitted for the detection technology we used and reduce risks of tag loss.\u003c/p\u003e \u003cp\u003eIndeed, the PIT tag need to be in a particular orientation when going through the antenna to maximize detection probability. Depending on the size of the access tunnel or individual walking physiology, the bird\u0026rsquo;s leg might not have the right orientation. PIT tags oriented perpendicularly to the magnetic field induced by the antenna would have a low detection probability, which could end up in data loss. This could be the reason why individuals with neck implants are detected a higher number of times each night. This could also be attributed to a difference in individual behavior but our data don't allow us to determine this. During the next season, several burrows will be monitored constantly with infrared cameras which will help us understand that phenomenon better. Lastly, detecting the PIT tag with a handheld detector through the opening atop the nest box would be much simpler when implanted in the back than attached on the leg.\u003c/p\u003e \u003cp\u003eStudies report various loss rates for subcutaneously implanted pit tags. The size of the bird and the injection method seem to be important factors (Bonter and Bridge \u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e2011\u003c/span\u003e). However, the tag loss rate was 0% on our sample (n\u0026thinsp;=\u0026thinsp;38). In addition, for diving species, subcutaneous tagging might help decrease the added drag, as internal implantation of tags generally causes reduced impacts (Wilson et al. \u003cspan citationid=\"CR51\" class=\"CitationRef\"\u003e1986\u003c/span\u003e; White et al. \u003cspan citationid=\"CR49\" class=\"CitationRef\"\u003e2013\u003c/span\u003e; Evans et al. \u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e2020\u003c/span\u003e). For example, positioning tags on the leg or the tail can cause instability (Vandenabeele et al. \u003cspan citationid=\"CR44\" class=\"CitationRef\"\u003e2014\u003c/span\u003e; Elliott \u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e2016\u003c/span\u003e). A study on crested auklets (\u003cem\u003eAethia cristatella\u003c/em\u003e) showed that a tarsus mounted tracking device (1% of the bird body mass) changed the behavior and at sea survival of marked individuals (Robinson and Jones \u003cspan citationid=\"CR35\" class=\"CitationRef\"\u003e2014\u003c/span\u003e). Similarly, increasing buoyancy or mass via a leg-mounted tag altered the dive behaviour of thick-billed murres (\u003cem\u003eUria lomvia\u003c/em\u003e; Elliott et al. \u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e2007\u003c/span\u003e), and attaching a leg-mounted tag for a year increased stress (corticosterone) in the same species (Elliott et al. \u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e2012\u003c/span\u003e). The mass of the 3D-printed leg band and PIT tag we used in our study was around 1g (\u0026asymp;\u0026thinsp;0.2% of the body mass), yet it could still have undesirable effects that we can avoid with subcutaneous implants.\u003c/p\u003e \u003cp\u003eHowever, this statement has to be taken cautiously as all tags should be considered to have an impact even if they are hard to detect (Elliott \u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e2016\u003c/span\u003e). The impact of such small devices might be particularly hard to detect as their mass are negligible. They could still have some long-term negative impact on survival (some marked individuals could suffer lesions from the tag migrating in the body) or may affect reproduction during subsequent years. For this reason, it is important to carry this study during several years before concluding on potential PIT tagging effects. Nonetheless, PIT tagging reduces disturbance on birds compared to manual burrow checks and GPS tagging due to decreased human presence on colonies. Thus, combining PIT tagging and automatic detection devices is a valuable method in studying sensitive seabird species during their breeding season.\u003c/p\u003e \u003cp\u003eSeveral detectors revealed individuals visiting alternate burrows in our study. This behavior has been observed in Leach\u0026rsquo;s storm-petrel (Zangmeister et al. \u003cspan citationid=\"CR53\" class=\"CitationRef\"\u003e2009\u003c/span\u003e) but not in the rhinoceros auklet. This phenomenon is unlikely to be due to a bird seeking for extra pair copulation, as data were collected late in the breeding season. One possibility is that those extra burrow visits could be attempts at kleptoparasitism (Senzaki et al. \u003cspan citationid=\"CR38\" class=\"CitationRef\"\u003e2014\u003c/span\u003e). Monitoring intra-specific kleptoparasitic behaviors could be a way to monitor ecosystem health via food shortages. Indeed, this behavior is most likely to happen when food availability is scarce (Beintema \u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e1997\u003c/span\u003e; Ashbrook et al. \u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2008\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eThis experiment also revealed that parents could come back to a burrow even after the chick disappeared. During productivity checks, we found several burrows without a chick that had one before. We considered the absence of a chick as proof of nest abandonment by the parents, yet no corpse was found in the burrow. In two cases, the parents came back to the nest after we concluded the burrow was abandoned. In one case, both parents had a nest attendance pattern similar to successfully breeding birds even if the chick was considered dead two weeks previously. Clearly, auklets continue visit their burrows even after chicks are dead.\u003c/p\u003e \u003cp\u003eThese observations highlight the potential of PIT tagging to bring more knowledge on certain species. There is growing evidence that, even if monitoring seabird species gives us access to helpful data in understanding their biology and the state of their environment, monitoring is done at the expense of their fitness. This problem is concerning, especially during long studies that could have negative long-term carryover effects on populations. In extreme cases, researchers could be missing important factors that would be otherwise demonstrated in an undisturbed population. PIT tagging could be used extensively in sensitive seabird species and in the light of our results and previous ones, should be considered for rhinoceros auklets, other puffins and other burrow-nesting species.\u003c/p\u003e \u003cp\u003eIn conclusion, PIT tagging rhinoceros auklets nesting in artificial burrows is a promising way to monitor their behavior, breeding outcomes and long-term survival while having the least possible disturbance. This technique could be applied to other sensitive seabird species with a similar biology like tufted puffins (\u003cem\u003eFratercula cirrhata\u003c/em\u003e). By replacing usual nest monitoring with automatic PIT tag recording, we reduce disturbance and probability of burrow collapse due to less frequent visits.\u003c/p\u003e"},{"header":"Declarations","content":"\u003cp\u003e\u003cstrong\u003eAcknowledgements\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eWe thank David Jadhon, Stella Solasz, Gabrielle Denis and Haley Gee for assistance with field work.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eFunding\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe research was funded by the Natural Sciences \u0026amp; Engineering Research Council of Canada, GulfWatch Alaska and Environment \u0026amp; Climate Change Canada.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eCompeting Interests\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe authors have no relevant financial or non-financial interests to disclose\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAuthors Contributions\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eLeo Marcouillier,\u0026nbsp;Shannon Whelan, Kyle H. Elliott contributed to the study conception and design. The detectors that made this study possible were built by Dave Fifield. Material preparation and data collection were performed by Leo Marcouillier, Elliane Miranda, Shannon Whelan and Chinatsu Nakajima. Analysis were performed by Leo Marcouillier. The first draft of this manuscript was written by Leo Marcouillier and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eData Availability\u003c/strong\u003e\u003c/h4\u003e\n\u003cp\u003eThe datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eEthics approval\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eAll activities were approved by the McGill Animal Use Protocol 2016-7814 and via permits from the US Fish \u0026amp; Wildlife Service and the Alaska Department of Fish \u0026amp; Game.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAuthors and affiliations\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eLeo Marcouillier\u003csup\u003e1\u003c/sup\u003e, Eliane Miranda\u003csup\u003e1\u003c/sup\u003e, Shannon Whelan\u003csup\u003e1\u003c/sup\u003e, Dave Fifield\u003csup\u003e2\u003c/sup\u003e, Scott Hatch\u003csup\u003e3\u003c/sup\u003e, Akiko Shoji\u003csup\u003e4\u003c/sup\u003e, Chinatsu Nakajima\u003csup\u003e4\u003c/sup\u003e and Kyle H. Elliott\u003csup\u003e1\u003c/sup\u003e\u003c/u\u003e\u003c/p\u003e\n\u003cp\u003eCorresponding author : L\u0026eacute;o Marcouillier : [email protected] \u0026nbsp; \u0026nbsp; \u0026nbsp; \u0026nbsp; \u0026nbsp; \u0026nbsp; \u0026nbsp;\u0026nbsp;\u003c/p\u003e\n\u003cp\u003e\u003csup\u003e1\u0026nbsp;\u003c/sup\u003eDepartment of Natural Resource Sciences, McGill University, Montr\u0026eacute;al, Canada\u003c/p\u003e\n\u003cp\u003e\u003csup\u003e2\u003c/sup\u003e Environment and Climate Change Canada, Mount Pearl, Canada\u003c/p\u003e\n\u003cp\u003e\u003csup\u003e3\u0026nbsp;\u003c/sup\u003eInstitute for Seabird Research and Conservation, United States of America\u003c/p\u003e\n\u003cp\u003e\u003csup\u003e4\u0026nbsp;\u003c/sup\u003eFaculty of Life and Environmental Sciences, University of Tsukuba, Japan\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\u003cli\u003e\u003cspan\u003eAckerman J, Adams J, Takekawa J, Carter H, Whitworth D, Newman S, Golightly R, Orthmeyer D (2010) Effects of radiotransmitters on the reproductive performance of Cassin\u0026rsquo;s Auklets. Wildl Soc Bull 32:1229\u0026ndash;1241. \u003cspan class=\"ExternalRef\"\u003e\u003cspan class=\"RefSource\"\u003ehttps://doi.org/10.2193/0091-7648(2004)032[1229:EOROTR]2.0.CO;2\u003c/span\u003e\u003cspan address=\"10.2193/0091-7648(2004)032[1229:EOROTR]2.0.CO;2\" targettype=\"DOI\" class=\"RefTarget\"\u003e\u003c/span\u003e\u003c/span\u003e\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eAshbrook K, Wanless S, Harris MP, Hamer C K (2008) Hitting the buffers: conspecific aggression undermines benefits of colonial breeding under adverse conditions. 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J Field Ornithol 80:373\u0026ndash;379. \u003cspan class=\"ExternalRef\"\u003e\u003cspan class=\"RefSource\"\u003ehttps://doi.org/10.1111/j.1557-9263.2009.00243.x\u003c/span\u003e\u003cspan address=\"10.1111/j.1557-9263.2009.00243.x\" targettype=\"DOI\" class=\"RefTarget\"\u003e\u003c/span\u003e\u003c/span\u003e\u003c/span\u003e\u003c/li\u003e \u003c/ol\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":false,"highlight":"","institution":"","isAcceptedByJournal":true,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":true,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"marine-biology","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"mabi","sideBox":"Learn more about [Marine Biology](https://www.springer.com/journal/227)","snPcode":"227","submissionUrl":"https://submission.nature.com/new-submission/227/3","title":"Marine Biology","twitterHandle":"","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"em","reportingPortfolio":"Springer Hybrid","inReviewEnabled":true,"inReviewRevisionsEnabled":false},"keywords":"","lastPublishedDoi":"10.21203/rs.3.rs-3112880/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-3112880/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003eInvestigator disturbance while monitoring seabirds often results in lower survival rates and breeding success, leaving lasting negative impacts on the population and biased observations. Puffins, in particular, are more sensitive to investigator disturbance than many other seabirds, and researchers must seek to decrease their disturbance and time spent at puffin colonies. Radio-Frequency Identification (RFID) via Passive Integrated Transponder (PIT) tags is an inexpensive and reliable way to identify individuals when coupled with automated RFID detectors, potentially avoiding the need for recapture for nocturnal seabirds. PIT tags either can be implanted subcutaneously or attached externally to leg bands, but it is unclear which method causes lower disturbance. To examine the impact of PIT tagging on rhinoceros auklets (\u003cem\u003eCerorhinca monocerata\u003c/em\u003e; a member of the puffin clade) nesting in artificial burrows on Middleton Island, Alaska, during the 2022 breeding season, we monitored burrow entrances with automated recording RFID readers to collect presence and nest attendance data. PIT tagged and control birds had similar breeding success and chick growth rates. Birds tagged externally were detected less often than birds marked with a subcutaneous implant. We conclude that PIT tagging on the rhinoceros auklet is a relatively non-invasive method for seabird monitoring, and that subcutaneous implants doesn't cause more disturbance than external attachment.\u003c/p\u003e","manuscriptTitle":"PIT tagging does not measurably reduce reproductive success in sensitive burrow-nesting seabirds","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2023-07-12 14:50:57","doi":"10.21203/rs.3.rs-3112880/v1","editorialEvents":[{"type":"communityComments","content":0},{"type":"decision","content":"Revise and Resubmit","date":"2023-08-13T11:21:53+00:00","index":"","fulltext":""},{"type":"reviewerAgreed","content":"","date":"2023-07-22T08:06:55+00:00","index":0,"fulltext":""},{"type":"reviewersInvited","content":"","date":"2023-07-08T00:03:09+00:00","index":"","fulltext":""},{"type":"editorAssigned","content":"","date":"2023-07-06T05:10:37+00:00","index":"","fulltext":""},{"type":"submitted","content":"Marine Biology","date":"2023-06-26T20:59:55+00:00","index":"","fulltext":""}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"marine-biology","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"mabi","sideBox":"Learn more about [Marine Biology](https://www.springer.com/journal/227)","snPcode":"227","submissionUrl":"https://submission.nature.com/new-submission/227/3","title":"Marine Biology","twitterHandle":"","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"em","reportingPortfolio":"Springer Hybrid","inReviewEnabled":true,"inReviewRevisionsEnabled":false}}],"origin":"","ownerIdentity":"a2eb5436-da83-4f7a-bb0f-544101e9ce88","owner":[],"postedDate":"July 12th, 2023","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"published-in-journal","subjectAreas":[],"tags":[],"updatedAt":"2024-02-26T15:05:18+00:00","versionOfRecord":{"articleIdentity":"rs-3112880","link":"https://doi.org/10.1007/s00227-023-04387-x","journal":{"identity":"marine-biology","isVorOnly":false,"title":"Marine Biology"},"publishedOn":"2024-02-22 15:01:20","publishedOnDateReadable":"February 22nd, 2024"},"versionCreatedAt":"2023-07-12 14:50:57","video":"","vorDoi":"10.1007/s00227-023-04387-x","vorDoiUrl":"https://doi.org/10.1007/s00227-023-04387-x","workflowStages":[]},"version":"v1","identity":"rs-3112880","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-3112880","identity":"rs-3112880","version":["v1"]},"buildId":"_2-kVJe1T_tPrBINL-cwx","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}