Elsevier

Fisheries Research

Volume 219, November 2019, 105325
Fisheries Research

Sex-specific probability of PIT tag retention in a cyprinid fish

https://doi.org/10.1016/j.fishres.2019.105325Get rights and content

Highlights

  • 2312 cyprinid fish (asp Leuciscus aspius) were tagged and tracked up to five years.

  • long-term retention rates of PIT-tags were assessed.

  • the female tag retention rate was significantly lower than the male retention rate.

  • PIT-tags may leave the body during reproduction and cause bias in the data.

Abstract

The estimation of age- and sex-specific mortalities is essential for constructing fish life tables and subsequent population modelling. However, the ecological data behind these parameter estimates acquired in nature may be systematically biased by the methodology of the study. To demonstrate mark retention bias by the widely used passive integrated transponder tags (PIT tags), we analysed long-term data showing the probability of tag retention within the body cavity in relation to fish sex. We used the cyprinid fish asp (Leuciscus aspius) as a model species with a cystovarian type of ovulation (eggs do not enter the body cavity). Altogether, 2312 fish were tagged with PIT tags in 2014–2018 and fin clipped and monitored for up to five years. In this period, 583 asp were recaptured at least one year after tagging, and fish that lost their tags were identified by regenerated fin. Based on recaptured fish, we show that the female tag retention rate is significantly lower than the male retention rate (85.3% in females vs. 97.8% in males). Furthermore, we used portable antenna to detect expelled PIT tags and localized a higher number of expelled female PIT tags on the spawning ground in comparison with those from males (123 female vs. 6 male PIT tags). This study demonstrates that systematic bias may potentially occur since PIT tags may penetrate gonads and leave the body during reproduction. We encourage designing PIT tag monitoring studies with respect to potential unequal sex-specific tag retention capabilities to avoid drawing inaccurate conclusions from biased data.

Introduction

The development of passive integrated transponder tags (PIT tags) for marking animals represented a highly innovative approach that allowed the investigation of many aspects of animal ecology because it enabled the recognition of individual animals over long timescales (Acolas et al., 2007; Castro-Santos et al., 1996). From studying individual growth rates to animal migratory behaviour, this technology changed the characteristics that ecologists could explore since it was first used in 1984 (Chapman et al., 2012; Jepsen et al., 2002; Prentice and Park, 1984). Their small size, low price and indefinite operational lifetime led to rapid proliferation of PIT tags among biological disciplines (Gibbons and Andrews, 2004). PIT tagging has been chosen for the investigation of a variety of animal taxa, including invertebrates (Bubb et al., 2002), fish (Hulthén et al., 2017), amphibians (Pope and Matthews, 2001), reptiles (Jemison et al., 1995), birds (Boisvert and Sherry, 2000) and mammals (Clay et al., 2009), and this method has become a major individual marking technique, especially in aquatic environments (Cooke et al., 2013).

Apart from recognizing already-captured animals with a hand reader and detecting animals in close proximity to scientists using a backpack antenna reader (Roussel et al., 2000), PIT tagged animals can be automatically detected in a laboratory or in natural environments using stationary detection systems that are installed in defined pathways of investigated species (Bond et al., 2018; Riley et al., 2010; Zydlewski et al., 2001). PIT tags do not have their own energy for signal emission as do tags for active telemetry (Bond et al., 2007; Zydlewski et al., 2006). Hence, to be detected, the PIT tag must be located close to the reader’s electromagnetic field. If present in the field, the PIT tag is charged and sends a unique code back to the reader (Enders et al., 2007).

The ability to scan wider animal pathways using PIT tags is in high demand, particularly because one of the major PIT tag applications is related to fish migration studies, e.g., effectiveness of fish ladders and usage of migratory pathways. Furthermore, the aim of monitoring fish movement is very challenging in large rivers (Lucas and Baras, 2001; Silva et al., 2018). Because the major limitation became the reading range of the PIT tag, larger PIT tags with longer antennas and reading ranges were produced and enabled the construction of river-wide stationary systems. This allowed us to broaden the applicability of the methodology to a wider array of model systems (Burnett et al., 2013).

However, the demand for larger tag usage changed the technique of inserting PIT tags into fish: while small PIT tags (8–12 mm length) were traditionally injected in dorsal muscles, larger PIT tags (23–32 mm length) must be inserted in the body cavity due to their larger size (Bateman and Gresswell, 2006; Skov et al., 2005). While tags inserted in dorsal muscles usually have high retention rates, the larger tags that are inserted in the body cavity of larger fish may have lower success rates (Cooke et al., 2011; Hooley-Underwood et al., 2017). The potential causes for this lower success rate might be fish exposure to high flow rates, which can cause tags to be expelled, or reproductive expulsion of a tag out of the fish body (Bateman et al., 2009; Dieterman and Hoxmeier, 2009; Meyer et al., 2011). Tag expulsion can potentially lead to unwanted bias produced by PIT tagging data, especially if the expulsion probability is not equal for all individuals within the tagged sample of the population.

While many PIT tag studies focus their attention on the species level, interesting questions can be raised on the level of individual variation (Adriaenssens and Johnsson, 2013; Bolnick et al., 2011; Hulthén et al., 2017). Sex is an important factor determining individual behavioural traits in fishes (Jonsson et al., 1991; Morbey and Ydenberg, 2001). Hence, to acknowledge differences between male and female behavioural traits, it is necessary to distinguish between sexes, which for many fish species, is possible only during the spawning period (Hulthén et al., 2014; Wootton and Smith, 2015). In such a study, especially if the aim is to assess the life-history characteristics of a given fish species, either tagging methodology should be equally efficient for both sexes, or the potential bias must be estimated and accounted for in the subsequent data handling. Sex-specific retention rates of PIT-tags can cause bias estimates of the survival rates of males and females, which can directly affect future management decision of species under interest.

Despite the common use of PIT tags in current research, scientists have paid little attention to the potential bias resulting from the different PIT tag retention probabilities between sexes during the reproductive period (Meyer et al., 2011). Among fishes, PIT tag studies have largely focused on salmonids, which are unique due to their secondary gymnovarian type of ovulation. The oviducts have been secondarily lost; thus, the eggs are shed into the peritoneal cavity and then spawned (Bromage et al., 1992; Helfman et al., 2009). Hence, it seems that salmonids have a much higher chance of shedding the PIT tag out with the eggs relative to most other fish species, which have a cystovarian type of ovulation. In these fishes, the eggs are spawned via the oviduct, and eggs do not enter the peritoneal cavity (Helfman et al., 2009; Santos et al., 2006).

To test whether females of species with cystovarian ovulation have a higher probability of tag loss during reproduction than males, we performed a study with a model species, the cyprinid fish asp (Leuciscus aspius), which inhabits central and eastern Europe. Asp is a long-lived iteroparous fish that inhabits lowland freshwaters and migrates for reproduction in fast-flowing waters (Šmejkal et al., 2018, 2017). Fish were annually caught close to their spawning ground and double-marked with PIT tags and fin-clipping for five consecutive seasons. The goal of this study was to analyse whether there was any difference in PIT tag retention probabilities related to fish sex using mark-recapture data and manual scanning of the spawning ground for expelled PIT tags. Apart from fish sex, we also tested the influence of water temperature at the tagging due to its importance in infection risk and its potential influence on the PIT tag expulsion probability via scar wound (Cooke et al., 2011) and fish length at the tagging, which was suggested to influence PIT tag retention rates (Dieterman and Hoxmeier, 2009).

Section snippets

Studied species and site

The study site was located in the main tributary of the Želivka Reservoir (39 km long, 1602 ha; 49°578497′ N, 15°251671′ E; Czech Republic). Asp migrate for reproduction in the early spring, and the spawning season is when the population can be sampled, PIT tagged and detected by passive telemetry systems. The spawning ground is approximately 100 m long in the tributary, with a water flow ranging between 0.1 and 0.4 m × s−1, and this site represents the only spawning ground of a large asp

Results

In total, 1235 males and 1077 females were tagged in all years combined. On the spawning ground, 48, 109, 171 and 216 asp individuals with retained PIT tags were recaptured from 2015 to 2018, respectively (Table 1). Furthermore, in these spawning seasons, 8 males and 31 females were captured and identified as marked due to the presence of a regenerated fin, but the PIT tag had been expelled (Table 2). The PIT tag retention probability was significantly different between sexes, and females had a

Discussion

This study suggests that females have a higher probability of expelling internally implanted PIT tags than do males. We identified a higher proportion of recaptured females with absent PIT tags in all years of the study in comparison with males in 2015–2018, and we verified the result by determining number and the actual location of the expelled PIT tags in the spawning ground. While the expulsion rate of tags inserted in the body cavity is generally not high in laboratory studies (Bateman and

Authors’ contributions

MŠ, JK and JD designed the study. MŠ, PB, DB, JD, LV, ZS, LK and JK participated in the field work. PB, ZS, DB and MŠ conducted the statistical analysis and visualized the results. MŠ wrote the first draft. All authors contributed substantial feedback during manuscript preparation. The authors declare no conflict of interest.

Acknowledgements

We thank Tomáš Kolařík, Zdeněk Popelka, Vladislav Draštík and other FishEcU members for their assistance during field work. Special thanks go to Vilém Děd, who structured and extracted data from the database. This research was supported by NAZV projectQJ1620240 (Application of “top-down” biomanipulation to reduce eutrophication caused by agriculture in reservoirs), by NAZV project “Aquaculture of rheophilous fish” (No. QK1920326), by Czech Academy of Sciences (ROZE project, Strategy AV 21) and

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