Satellite Tagging and Biopsy Sampling of Killer Whales at Subantarctic Marion Island: Effectiveness, Immediate Reactions and Long-Term Responses

Remote tissue biopsy sampling and satellite tagging are becoming widely used in large marine vertebrate studies because they allow the collection of a diverse suite of otherwise difficult-to-obtain data which are critical in understanding the ecology of these species and to their conservation and management. Researchers must carefully consider their methods not only from an animal welfare perspective, but also to ensure the scientific rigour and validity of their results. We report methods for shore-based, remote biopsy sampling and satellite tagging of killer whales Orcinus orca at Subantarctic Marion Island. The performance of these methods is critically assessed using 1) the attachment duration of low-impact minimally percutaneous satellite tags; 2) the immediate behavioural reactions of animals to biopsy sampling and satellite tagging; 3) the effect of researcher experience on biopsy sampling and satellite tagging; and 4) the mid- (1 month) and long- (24 month) term behavioural consequences. To study mid- and long-term behavioural changes we used multievent capture-recapture models that accommodate imperfect detection and individual heterogeneity. We made 72 biopsy sampling attempts (resulting in 32 tissue samples) and 37 satellite tagging attempts (deploying 19 tags). Biopsy sampling success rates were low (43%), but tagging rates were high with improved tag designs (86%). The improved tags remained attached for 26±14 days (mean ± SD). Individuals most often showed no reaction when attempts missed (66%) and a slight reaction-defined as a slight flinch, slight shake, short acceleration, or immediate dive-when hit (54%). Severe immediate reactions were never observed. Hit or miss and age-sex class were important predictors of the reaction, but the method (tag or biopsy) was unimportant. Multievent trap-dependence modelling revealed considerable variation in individual sighting patterns; however, there were no significant mid- or long-term changes following biopsy sampling or tagging

Selection criteria for multievent capture recapture models of sighting histories of killer whales at Marion Island: long-term (up to 24 months) responses following sampling (tagging or biopsy) attempts.

<p>‘Season’ refers to the same seasonality affect for all individuals. ‘DH(1).season’ refers to seasonality applying only to one of two hidden mixture groups (suggesting ‘resident’ and ‘migrant’ animals) while ‘DH(2).season’ refers to seasonality applying to all individuals but independently for two hidden groups (suggesting variation between individuals). ‘trap’ refers to a trap-dependence effect, ‘sampling’ refers to a sampling effect and ‘t_{2008–2011;2011–2013}’ accounts for two periods with differing field effort.</p><p>Notes: ^aĉ = 1.75.</p><p>Selection criteria for multievent capture recapture models of sighting histories of killer whales at Marion Island: long-term (up to 24 months) responses following sampling (tagging or biopsy) attempts.</p

Model selection for the generalized linear models (GL Ms) used to describe factors influencing the probability of hitting the target animal (<i>hit/miss</i>) during a sampling attempt.

<p>The full model was <i>hit/miss ∼experience + biopsy/tag + range + arbalester</i>. Only the predictor variables included in each model are shown.</p><p>Notes: ^anumber of parameters; ^bsmall sample corrected Akaike Information Criterion; ^cdifference between the AIC_c score of the model in question and the best model; ^dAkaike weight: relative likelihood of model in question divided by the sum of relative likelihoods for all models.</p><p>Model selection for the generalized linear models (GL Ms) used to describe factors influencing the probability of hitting the target animal (<i>hit/miss</i>) during a sampling attempt.</p

Immediate behavioural reactions to satellite tagging and biopsy sampling.

<p>Frequency of different immediate behavioural reactions of killer whales at Marion Island to tagging and biopsy sampling.</p

Satellite tagging of an adult male killer whale.

<p>Still frame from a point of view video showing satellite tagging of an adult male killer whale (M007) at Marion Island. The tag can be seen in the dorsal fin.</p

Description of scores used to assess the immediate reactions of killer whales to biopsy sampling or tagging.

<p>Description of scores used to assess the immediate reactions of killer whales to biopsy sampling or tagging.</p

Number of biopsy sampling and satellite tagging attempts on killer whales at Marion Island.

<p>Notes: ^aFollowing <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0111835#pone.0111835-Best1" target="_blank">[24]</a>; ^bHit and tissue sample for biopsy sampling, hit and attach for satellite tagging; ^cTags attached, but did not necessarily penetrate properly.</p><p>Number of biopsy sampling and satellite tagging attempts on killer whales at Marion Island.</p

Selection criteria for multievent capture recapture models of sighting histories of killer whales at Marion Island: mid-term (1 month) responses following sampling (tagging or biopsy) attempts.

<p>‘Season’ refers to the same seasonality affect for all individuals. ‘DH(1).season’ refers to seasonality applying only to one of two hidden mixture groups (suggesting ‘resident’ and ‘migrant’ animals) while ‘DH(2).season’ refers to seasonality applying to all individuals but independently for two hidden groups (suggesting variation between individuals). ‘trap’ refers to a trap-dependence effect, ‘sampling’ refers to a sampling effect and ‘t_{2008-2011;2011-2013}’ accounts for two periods with differing field effort.</p><p>Notes: ^aĉ = 1.75.</p><p>Selection criteria for multievent capture recapture models of sighting histories of killer whales at Marion Island: mid-term (1 month) responses following sampling (tagging or biopsy) attempts.</p

Model selection for the generalized linear mixed effects models (GLMMs) used to describe the reaction of killer whales to biopsy sampling and tagging.

<p>The full model was <i>reaction ∼class + hit/miss + biopsy/tag + (1|individual)</i>, where <i>reaction</i> was the response variable and <i>(1|individual)</i> denoted a random effect. All models included the random effect; only the predictor variables included in each model are shown.</p><p>Notes: ^anumber of parameters; ^bsmall sample corrected Akaike Information Criterion; ^cdifference between the AIC_c score of the model in question and the best model; ^dAkaike weight: relative likelihood of model in question divided by the sum of relative likelihoods for all models.</p><p>Model selection for the generalized linear mixed effects models (GLMMs) used to describe the reaction of killer whales to biopsy sampling and tagging.</p

Wildlife Computers SPOT5 satellite-linked tag with attachment darts.

<p>The inset shows the tag in a deployment cup, attached to a crossbow bolt with float.</p