Evaluation of passive integrated transponders for abalone: tag placement, retention, and effect on survival.
KEY WORDS: pinto abalone, Haliotis kamtschatkana kamtschatkana, passive integrated transponders, tag
Mark-recapture--a system in which animals are removed physically from their environment, tagged with distinct numbers, and recovered in subsequent surveys--is a standard method in conservation biology to estimate population size, track migration patterns, and assess growth and mortality (Gibbons & Andrews 2004, Henry & Jarne 2007). Despite the fact that shelled gastropods can be tagged with limited invasiveness, a robust tagging technique is lacking (Henry & Jarne 2007), in part because of the limitations of cost, tag retention, effect on the animal, and efficiency of search for tagged animals. Existing tagging methods for marine gastropods, including abalone, share these limitations.
A robust tagging system would provide valuable data on abalone population dynamics. Abalone species worldwide are in decline, including pinto, white, and black abalone (Hobday et al. 2000, Rothaus et al. 2008, Neuman et al. 2010, Bouma et al. 2012). Many abalone species are surveyed actively by managers and remain the focus of restoration activities (Watson & Vadopalas 2009). Enumeration of abalone in the field is challenging because they are often nested in crevices of rocky substrate or are otherwise out of reach. Distinguishing individuals under these circumstances will empower researchers to detect abalone in situ. Thus, requirements for a successful tagging system for pinto abalone include the following characteristics: high retention rate, low impact on animal survival and health, and detectable under field conditions.
Although noninvasive individual tags such as plastic disks and numbered washers have been used to track growth and movement of shelled gastropods such as abalone, these tags have limited effectiveness (Catchpole et al. 2001, Henry & Jarne 2007). Such tags are difficult to read and may be overlooked at unacceptably high rates when the marked animal is in a cryptic microhabitat. Tags may be dislodged from the animal or may become unreadable without significant effort on the part of the observer as a result of erosion, decay, or encrusting epibionts, and may be difficult for divers to visualize underwater (Henry & Jarne 2007). Genetic tagging is feasible but can be costly and it does not provide the capability of immediate identification in the field (Henry & Jarne 2007).
Passive integrated transponder (PIT) technology may be a viable alternative to traditional tagging methods (Gibbons & Andrews 2004) if effects on the animal are minimal, tag retention is high, and the use of PITs increases the efficiency of search for tagged animals. PIT tags are small, biocompatible, glass-encapsulated integrated circuits that are activated by the PIT tag reader to relay the unique identifier number sequence (Wyneken et al. 2010). Since their first use in the mid 1980s (Gibbons & Andrews 2004), PITs have been used in a variety of taxa to answer a range of questions, from physiological to behavioral. PIT tags may increase identification efficiency greatly for marine gastropods as a result of their nonvisual detection technology, significant potential for longevity, and the potential to obviate recapture. PIT tags are essentially permanent if retained and can last up to 75 y or more (Biomark, Boise, ID), increasing accuracy and eliminating the need for retagging. In addition, the unique identifier code for each PIT tag reduces substantially the chance of identification error by storing tag number data in the PIT reader.
To address the limitations of traditional tagging methods, PITs were used experimentally to tag pinto abalone. We evaluated PIT tagging methods on both small adult (age, 3.5 y; mean initial shell length (SL, where SL is the maximum linear dimension of the elliptical shell), 59.3 mm; range, 40.1-75.5 mm) and juvenile (age, 2 y; mean initial SL, 23.6 mm; range, 17.5-32.1 ram) pinto abalone by assessing tag retention and tagging effects on growth and survival. Three methods were evaluated on small adult animals, including attachment of PITs to the dorsal exterior and ventral anterior of the shell, and foot muscle injection. PIT tag attachment on the ventral anterior of the shell was also evaluated in juvenile pinto abalone.
MATERIALS AND METHODS
Experimental Animal Care
Larval pinto abalone were produced and reared in a hatchery setting at the NOAA Mukilteo Research Station in Washington state. Abalone were held in culture tanks that received 20-[micro]m-filtered, 8-14[degrees]C, ~30 PSU seawater, and were fed ad libitum naturally occurring benthic diatoms and macroalgae Nereocystis leutkeana and Palmaria mollis. Small adult abalone (adults; age, 3.5 y; mean initial SL, 59.3 mm; range, 40.1-75.5 mm) produced during fall 2007, including both males (n = 17) and females (n = 23), were used in trial 1. Juvenile abalone (juveniles; n = 42; age, 2 y; mean initial SL, 23.6 mm; range, 17.5-32.1 mm) produced in 2009 were used in trial 2. The number of individuals in each trial was determined by the number of individuals available in each age class at the NOAA Mukilteo Research Station hatchery. For each trial described next, holding tanks were maintained at ambient temperatures from 8-14[degrees]C, with a mean temperature of 12[degrees]C. Handling, including tank cleaning, was minimized for 4 days after tagging to avoid further stress. Subsequent tank cleaning and feeding were conducted weekly.
Trial 1: Small Adults
Abalone were maintained in a 180-L fiberglass tank. Abalone (n = 40) were removed from the tank and placed into submerged mesh bags to facilitate handling. Each animal was tagged initially with a 2-mm bee tag (The Bee Works, Orillia, Ontario, Canada) attached near the spire with cyanoacrylate glue (Zap-a-Gap; Pacer Technology, Rancho Cucamonga, CA). Abalone were assigned randomly to 4 groups (n = 10 each) representing 3 tag treatments and 1 untagged control. After bee tag placement, control animals were returned to the common tank. We did not control separately for glue effects. PIT tags (9-mm full duplex, HPT9; Biomark) were adhered to the dorsal exterior of the shell in the groove formed below the respiratory pores (exterior; Fig. 1), the ventral anterior along the leading edge (interior; Fig. 1) of the shell using IC-GEL (Bob Smith Industries, Inc., Atascadero, CA), and injected into the lateral side of the foot muscle with a 12-gauge needle (MK 10 Implanter, N215 needles; Biomark) (tissue, Fig. 1) in respective treatment groups. The injection site was sealed with cyanoacrylate glue. After tagging, abalone were placed in a 10-L bucket of seawater to cure the glue. After tagging, the individual identifier number from each tagged abalone was read with a PIT tag reader (601 Handheld Reader; Biomark), recorded, and matched with the individual's bee tag number. All abalone were returned to the 180-L common tank after tagging was complete. Survival and tag loss were monitored weekly for 15 mo. Initial and final SL was recorded for each individual.
Trial 2: Juveniles
Juvenile abalone (n = 42) were pretagged with bee tags as described earlier. Juveniles were assigned randomly to 2 groups (n = 22 PITs, n = 20 control). Those in the PIT tag group were tagged by gluing individual PIT tags to the ventral anterior of the shell as described earlier. After tagging, the individual identifier number from each tagged abalone was read with the PIT tag reader, recorded, and matched with the individual's bee tag number. All abalone were returned to their culture tank for the duration of the study. Survival and tag loss were monitored weekly for 6 mo. Initial and final SL were recorded for each individual.
Chi-square tests with Yate's continuity correction were used to determine whether survival and tag retention proportions differed among treatment groups, and to compare tag retention and mortality proportions between small adults and juveniles. To evaluate relative growth rate (RGR = [ln SL2 - In SL1]/ [[increment of Time]]) differences among treatments in trial 1, we used single-factor analysis of variance (ANOVA).
Trial 1: Small Adults
Tag retention differed significantly among groups (chi-square = 18.37, df = 2, P < 0.001). In PIT-injected abalone, tag retention was 10%. A single foot muscle tag remained in one abalone that later died after developing a large lesion protruding from the injection site (Fig. 2). Tag retention in internally and externally adhered PITs was 90% and 80%, respectively (Table 1).
Survival and Growth
Over a 15-mo observation period after tagging, 7 mortalities occurred. Mortalities occurred in all treatment groups except for the ventral anterior-adhered group. Mortalities occurred as follows: 1 animal in the externally adhered group, 4 in the injected group, and 2 controls. Survival was similar among treatments (chi-square = 6.06, df = 3, P = 0.11; Table 1). Despite significant differences in SL among treatments at the beginning and end of the experiment (ANOVA, F = 3.99, df = 3, P = 0.015; ANOVA, df = 3, F = 3.26, P = 0.04, respectively), RGRs were similar among treatments (ANOVA, F = 1.40, df = 3, P = 0.262).
Response to PITs Adhered to Ventral Anterior of Shell
After 37 days, 1 abalone had covered the ventral anterior-adhered PIT with mantle tissue, and newly deposited nacre was visible covering the tag (Fig. 3). Similar observations occurred during the subsequent 60 days. All ventral anterior-adhered PITs in the remaining abalone in this treatment group were covered in nacre after 3 mo.
Trial 2: Juveniles
Tag retention in juveniles was 86%; 3 of 22 juveniles lost their PIT (Table 1).
Survival and Growth
During the 6-mo observation period after tagging, 11 mortalities occurred. Mortalities occurred in both treatment groups, including 8 animals in the ventral anterior-adhered group and 3 controls. Survival was similar among treatments (chi-square = 0.57, df = 1, P = 0.45; Table 1). No growth analyses were possible for trial 2 because of initial size differences between control and treatment groups (average initial SL, 20.7 mm and 23.9 mm, respectively) confounding growth analyses as a result of ontogenetic growth rate differences.
Response to PITs Adhered to Internal Shell
On observation (day 63 after tagging), 8 animals had abnormal epipodial tissue near the tagging site. In the majority of tagged animals, mantle tissue was either receded or up against the tag. Only a single subject animal in trial 2 had moved mantle tissue over the tag and deposited nacre over the PIT tag. On final observation, 178 days after tagging, 7 animals had abnormal shell growth near the tagging site (Fig. 4).
Small Adult and Juvenile Comparison
For the ventral anterior-adhered PITs, tag retention proportions were the same between the small adults (90%) and the juveniles (86%; chi-square = 0.08, df = 1, P = 0.77). All tagged animals that died had retained their tag at the time of death. All small adults deposited nacre over PITs.
We developed a novel method for the attachment of PITs in abalone, and for the first time tested retention, growth, and mortality in a controlled environment. When PITs were applied to the ventral anterior shell in adult abalone, they became embedded in deposited shell (nacre), resulting in a high rate of tag retention and low associated mortality. Nacre-embedded tags decrease the probability of tag loss and likely reduce the possibility of tag damage from exposure.
Methods for tagging abalone have generally fallen into 2 categories (Prince 1991): tags applied with adhesives (Kraeuter et al. 1989, Debrot 1990, McShane & Smith 1992, Worthington et al. 1995, Henry & Jarne 2007) or tags secured to abalone respiratory pores (Prince 1991, Catchpole et al. 2001). Abalone have also been tagged chemically to alter shell color for identification of hatchery-reared individuals in the wild (Chick 2010). Henry and Jarne (2007) estimated that a tag loss rate of 0.01-0.1/mo is expected for most marking techniques, including adhesion of plastic tags, rivets, and various types of paint. Prince (1991) attached numbered disks to the respiratory pores of abalone with rivets, and observed tag losses of 4-35% over a 1-y period. Debrot (1990) tagged Cittarium pica, a marine snail, with a plastic disk glued with epoxy resin, and estimated a tag loss rate of 43% per year (Debrot 1990), which is much higher than the 10% tag loss we observed over 15 mo in small adults with ventral anterior-adhered PITs. Henry and Jarne (2007) hypothesized that tag loss in C. pica was a result of tag abrasion because of their crevice-dwelling habitat, similar to the habitat of many abalone species.
We found that abalone covered PIT tags with nacre, embedding the tag in the shell. Prince (1991) observed that 33% of animals that retained plastic rivet tags had covered the rivet with nacre after 1 y. In the current study, we observed 100% of the PITs embedded in nacre in the small adults after only 3 mo. The difference may be the result, in part, of the biocompatible characteristics of the glass encapsulation (Schott 2012) relative to nylon rivets, or the movement of the rivet against the respiratory pores. In freshwater mussels and the clam Mya arenaria, PITs inserted between the mantle and shell were also covered with nacre, further suggesting the possibility for long-term retention (Kurth et al. 2007; Hamilton & Connell 2009, respectively).
PITs circumvent many problems associated with visually encountering a variety of organisms and their tags in situ. Angeloni and Bradbury (1999) tagged the large marine ospithobranch Aplysia vaccaria with PITs, but did not record tag retention. Marine polychaetes were tagged successfully with coded microwire tags (Glycera dibranehiate and Nereis virens (Joule 1983)), as well as other marine invertebrates such as red king crabs (Paralithodes camtschaticus (Pengilly & Watson 1994)), lobsters (Homarus americanus (Ennis 1972), Panulirus argus (Sharp et al. 2000)), and prawns (Pandalus platyceros (Prentice & Rensel 1977)). Freshwater unionid mussels have also been tagged with PITs (Young & Isely 2008, Kurth et al. 2007, Wilson et al. 2011), resulting in 90-100% tag retention of externally attached PITs (Young & Isely 2008) and 75-100% tag retention of internally attached PITs (Kurth et al. 2007). Mussel reencounter rates were 72-80% with PIT technology compared with 30-47% by visual search methods (Kurth et al. 2007). Terrestrial invertebrates such as snails and beetles (Paryphanta busbyi watti and Plocamosthetus planiusculu, respectively (Lovei et al. 1997)), bees (Bombus terrestris and Apis mellifera (Riley et al. 1996)), ground beetles (Carabus coriaceus (Riecken & Raths 1996) and Calosoma affine (Wallin 1991)) have been tagged and tracked successfully with harmonic radar, a method similar to PIT tagging. In contrast to PITs, however, the reflected harmonic signal does not yield a unique identifier for each animal.
In the field, PITs have been used to tag black abalone (Haliotis craeherodii) by attachment to the external shell with both epoxy and cyanoacrylate cement. However, effectiveness was reduced by significant tag loss and consistent loss of PIT function after about 1 y (G. VanBlaricom, University of Washington, January 17, 2011, pers. comm.). Tags may have been rendered unreadable as a result of wave impact in the highly dynamic rocky intertidal habitat of black abalone (G. VanBlaricom, 2011, pers. comm.). Adult pink (Haliotis corrugata) and green (Haliotis fulgens) abalone have also been tagged experimentally by attaching PITs with marine epoxy (Z-SPAR Splash Zone; Simco Coatings, Inc., Los Angeles, CA) to the external dorsal shell underneath a numbered stainless steel washer (1. Taniguchi, California Department of Fish and Game, March 29, 2012, pers. comm.). If incorporation via nacre deposition is similar to our observations for pinto abalone, ventral anterior PIT placement may optimize high retention rates in black, green, and pink abalone, and may reduce the impact of wave forces on PITs. Retention and survival rates for the PIT tagging method we describe for pinto abalone compares favorably with traditional methods used to tag hardshell gastropods. Based on our results, the majority of tag loss is likely to occur during the first 3 mo. After nacre deposition, we observed no tag loss; thus, we expect further tag loss to be minimal.
PIT-tagged abalone have been located in the field using handheld readers in combination with metal detectors in intertidal habitats (G. VanBlaricom, 2011, pers. comm.), PIT detection units (Kurth et al. 2007), and custom readers, including a reader (FS2001F-ISO Reader; Biomark) inside a custom underwater housing (PREVCO Subsea LLC, Fountain Hills, AZ) with a waterproof cable to a racket-style antennae (I. Taniguchi, 2012, pers. comm.). We are currently developing a fully submersible PIT tag reader in which the reader board and reader are fully encased in a waterproof container.
PIT tagging may not be a viable option for juvenile or small abalone. Although we observed low tag loss and low mortality in juveniles, 7 of the tagged juveniles exhibited abnormal shell formation (Fig. 4) that was not reflected in final SL measurements. In small abalone, the relatively large tag size combined with insufficient mantle tissue to cover the PIT may preclude tag assimilation. Concurrent with our experiments, large adult pinto abalone (mean SL, 115 mm; n = 33) were also PIT tagged on the ventral anterior shell in 2011. After 6 mo, tag retention in this group was high (96%) and PITs were embedded in nacre (data not shown), illustrating the potential for tracking important broodstock in commercial and restoration abalone hatcheries.
A robust tagging system for pinto abalone would enable investigators to monitor the progress of restoration efforts that include aggregation and population supplementation, and to increase survey resolution for declining species, such as pinto abalone. In the short term, PIT tagging may be more expensive than some traditional methods (approximately $6/tag). However, PITs applied to the ventral anterior shell may ultimately prove cost-effective as a result of high retention and sustained readability. In addition, by obviating the need to encounter tags visually to confirm identification, PIT tags have the potential to increase the speed and resolution of surveys, providing valuable data on population dynamics in abalone species. Studies are underway to characterize PIT tag retention in natural habitats and to track adults reintroduced to the natural environment.
We thank T. Bennett for help with the development of an underwater PIT reader. We also thank G. VanBlaricom, K. Straus, E. Dorfmeier, J. Watson, and B. Sizemore for valuable editorial comments. We gratefully acknowledge P. Plesha, NOAA Mukilteo Research Station, and the School of Aquatic and Fishery Sciences (SAFS), University of Washington for use of facilities and equipment. This research was funded, in part, by a grant from the National Marine Fisheries Service, Proactive Conservation Program: Species of Concern, National Oceanic and Atmospheric Administration, U.S. Department of Commerce, under grant no. NA11NMF4720277, CFDA no. 11.472 to the Washington Department of Fish and Wildlife. The views expressed herein are those of the authors and do not necessarily reflect the views of NOAA or any of its subagencies. The U.S. government is authorized to reproduce and distribute for governmental purposes. Funding was also provided by the School of Aquatic and Fishery Sciences, University of Washington.
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J. R. HALE, (1) J. V. BOUMA, (2) B. VADOPALAS (1) * AND C. S. FRIEDMAN (1)
(1) University of Washington, School of Aquatic and Fishery Sciences, 1122 NE Boat Street, Seattle, WA 98105; (2) Puget Sound Restoration Fund, Pinto Abalone Recovery, 590 Madison A venue North, Bainbridge Island, WA 98110
* Corresponding author. E-mail: email@example.com
TABLE 1. Proportion survival and retention of PIT tags in pinto abalone, Haliotis kamtschatkana kamtschatkana. Group Treatment (n) Duration (mo) Retention Survival Small adult Injected (10) 15 0.10 0.60 Outside (10) 15 0.80 0.90 Inside (10) 15 0.90 1.00 Control (10) 15 -- 0.80 Juvenile Inside (22) 6 0.86 0.63 Control (20) 6 -- 0.85 Injected, tags inserted into the foot muscle; Inside, tags glued on the interior edge of the shell; Outside, tags glued to the exterior of the shell.
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|Author:||Hale, J.R.; Bouma, J.V.; Vadopalas, B.; Friedman, C.S.|
|Publication:||Journal of Shellfish Research|
|Date:||Aug 1, 2012|
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