Get 20M+ Full-Text Papers For Less Than $1.50/day. Start a 14-Day Trial for You or Your Team.

Learn More →

Testing tag attachments to increase the attachment duration of archival tags on baleen whales

Testing tag attachments to increase the attachment duration of archival tags on baleen whales Background: As biologging technology has advanced to study whale behavior, various tag attachment methods have been developed. Suction cup attachments were developed for short-term (<24 h) studies using high-resolution archival tags, and implantable or dart attachments were developed for long-term (months) studies using coarse- resolution satellite tags. The purpose of this study was to test various tag attachment configurations to increase the deployment duration of archival tags while minimizing potential physical impacts to the whale. Results: From 2013 to 2015, 31 humpback whales (Megaptera novaeangliae) and 20 blue whales (Balaenoptera mus- culus) were tagged, allowing us to test 10 tag attachment configurations, grouped as suction cup, suction cup with dart, two-dart configurations with petals, four-dart configurations, and four-dart configurations with petals. Dura- tions resulting from four-dart configurations with petals were greater than suction cup tags for humpback whales (P = 0.04). Durations resulting from four-dart configurations with petals were greater than all other tag attachment types for blue whales (P < 0.04). There was no difference in reaction to tagging by tag attachment type for humpback (P = 0.19) or blue whales (P = 0.24). Tags attached with titanium darts were recovered with 2 darts (5 %) lost and 31 petals (14 %) broken, whereas tags attached with stainless steel darts were recovered with 1 dart (3 %) lost and 2 petals (1 %) broken. Re-sights of three tagged animals up to 34 days after tags detached showed no sign of tearing or swelling at the tag site. Conclusions: Tag attachments using four darts with petals remained on whales the longest with no increase in reac- tion to tagging by either species. Heat-treated stainless steel darts resulted in equivalent tag attachment durations as titanium darts but with reduced petal breakage. Attachments with four darts, despite creating additional points of entry for potential bacterial transfer, did not produce signs of tearing or swelling on animals re-sighted up to 34 days after tagging. Attaching archival tags with four stainless steel darts with petals on baleen whales will allow for the collection of weeks of fine-scale data, allowing researchers to answer questions about foraging, daily activity, and diel trends. Keywords: Biologging, Long-term tag, Tag development, Baleen whale, Dive behavior technology has quickly advanced, integrating GPS, accel- Background erometers, magnetometers, pressure sensors, and acous- The first measurement of the maximum dive depth of a tic recorders that allow for the collection of biological, marine animal was recorded when a capillary-tube pres- environmental, and behavioral information on free rang- sure gauge was attached to a fin whale ( Balaenoptera ing marine animals [2–5]. physalus) with a harpoon [1]. Since then, biologging As new tag technology was being introduced, so were methods of tag attachment. Unlike turtles, pinnipeds, *Correspondence: angela@szesciorka.com and small odontocetes that could be captured and tagged Moss Landing Marine Laboratories, 8272 Moss Landing Rd, Moss using harnesses, rings, epoxies, and acrylic glues [e.g., Landing, CA 95039, USA Full list of author information is available at the end of the article © 2016 The Author(s). This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Szesciorka et al. Anim Biotelemetry (2016) 4:18 Page 3 of 12 6–11], large whales could not be captured and their The short 3-petal and long 6-petal Grade 4 titanium smooth, hairless, and regularly sloughed skin made epoxy darts (Fig.  2a, b) were manufactured by Wildlife Com- or glue methods impossible. This led to the development puters (Redmond, WA, USA) for the Low Impact Mini- of tag attachments that could be implanted into the bod- mally Percutaneous External-electronics Transmitter ies of larger cetaceans using modified crossbows or pneu - (LIMPET) system, based on designs developed by Russ matic guns [12, 13]. Andrews [20, 21]. Implantable tags were designed to pen- Implantable satellite tags allowed for long-term tag etrate the fascia and muscle layers of the whale, opening deployments (months) on whales, enabling researchers to up the possibility of bacterial transfer inside the body answer questions about distribution and movement [13– leading to inflammation and infection. To reduce poten - 15]. However, satellite transmissions can only send small tial physical impact on whales, the LIMPET darts do not amounts of compressed data at each uplink, which can exceed 8  cm in length so they do not penetrate beneath be affected by the number of satellites present at the time the blubber layer, which for humpback whales is ~15 cm of uplink and how long the animal remains at the surface deep [22], whereas implantable tags penetrate into the [16]. Using a combination of transmission to satellites blubber and into the muscle as deep as 30.5 cm [12, 13]. augmented with shore-receiving stations has allowed The backwards-facing petals of the titanium darts pro - some transmission of more detailed data [17]. Because vided anchoring when the tag penetrated the blubber bandwidth limitation results in coarse-resolution data, layer. For both long and short titanium darts, the pet- these tags are typically not suitable for fine-scale studies als were clipped to roughly two-thirds of their original of behavior. length and rounded to reduce potential tearing as the Another direction in tag attachment has been the use darts worked their way out of the animal. of suction cup-attached archival tags that do not pene- The short, conical, and triangular machinable certified trate the skin [18]. In addition to being readily available, 17-4 PH stainless steel darts were manufactured at Moss inexpensive, and easy to attach via crossbow or pole [19], Landing Marine Laboratories (Moss Landing, CA, USA; these tags were designed to collect data at high-sampling Fig.  2c–e). The long 3- and 6-petal machinable certified rates, allowing for the collection of fine-scale informa - 17-4 PH stainless darts (Fig. 2f, g) were manufactured by tion on behavior [16]. The tags needed to be recovered to American Benchmark Machine Works (Olympia, WA, retrieve the data, so they were not constrained by band- USA). These darts were designed to be similar to the width limits like satellite tags. However, because suc- titanium darts from the LIMPET system, but were con- tion cup-attached tags typically remained on for <24  h, structed using stainless steel, which is less brittle than researchers could not answer questions about fine-scale titanium. Welding petals onto the darts adds excess heat behavior at time scales of days to weeks. to the surface area of petals, creating weaknesses where The purpose of this study was to test various tag attach - breakage can occur. To decrease the risk of petal break- ment configurations, including methods typically used age from welding and lessen the effects of elongation with dart-attached satellite tags to increase the deploy- (how much the material stretches before breaking), the ment duration of archival tags, ultimately allowing for the darts were heat-treated at 1100 °F for 4 h. collection of high-resolution behavior data over interme- These tag attachment materials were tested in 10 con - diate time periods (days to weeks) compared with current figurations: (1) suction cup (rigid), (2) suction cup (semi - suction cup-attached archival tags (<24  h), while mini- rigid) with a short conical stainless steel dart, (3) two mizing the potential physical impacts to the whale. short (3 petals each) titanium darts, (4) two long (6 pet- als each) titanium darts, (5) four long stainless steel coni- Methods cal darts, (6) four stainless steel triangular darts, (7) two Tag attachment development short (3 petals each)/two long (six petals each) titanium The tag attachments tested in this study included vari - darts, (8) four long (6 petals each) titanium darts, (9) four ous configurations of suction cup (Fig.  1a), darted suc- long (3 petals each) stainless steel darts, and (10) four tion cup (Fig.  1b), two-dart configurations with petals long (6 petals each) stainless steel darts. To minimize (Fig. 1c), four-dart configurations (Fig.  1d), and four-dart bacterial transfer and risk of infection, the darts were gas configurations with petals (Fig.  1e). Individual tag attach- sterilized in ethylene oxide (Sequoia Veterinary Hospital; ment materials included two types of suction cup, two Redwood City, CA, USA), cleaned in 70 % rubbing alco- Grade 4 titanium darts, and five machinable certified hol, and coated with 7.5  % povidone-iodine (Betadine) 17-4 PH stainless steel darts (Table 1). surgical scrub solution before tagging. Rigid suction cups came from Canadian Tire (Toronto, The tag attachment methods were tested by attach - ON, USA; Fig. 1a), and semirigid suction cups came from ing a time-depth recorder (TDR) archival tag (Wildlife Cetacean Research Technology (Seattle, WA; Fig.  1b). Computers; Redmond, WA, USA) below the dorsal fin Szesciorka et al. Anim Biotelemetry (2016) 4:18 Page 4 of 12 Fig. 1 TDR tags with syntactic foam, radio transmitter and/or satellite tag, and tag attachment. a Suction cup attachment, b suction cup with dart attachment, c two darts with petals, d four darts with no petals, and e four darts with petals of humpback whales or on the dorsal ridge just forward Redmond, WA, USA), which weighed 53  g. The satel - the dorsal fin of blue whales. Tags were attached as high lite tag was programmed to transmit via the Argos sys- on each animal as possible to maximize reception of the tem, providing position estimates within 250 m when the satellite tag and VHF transmitter. The TDR’s dimensions tag was detached and floating at the water’s surface. The were 102  mm  ×  56  mm  ×  30  mm, and they weighed second recovery aid was a 10-g VHF transmitter (Series 225  g in air. The TDRs were glued into a syntactic foam MM100, Advanced Telemetry Systems Inc.; Isanti, MN, housing for floatation that varied in shape and weight. USA). Once within range of the tag’s last estimated posi- Total tag weight, including the syntactic foam, VHF, sat- tion, we used the pulse strength of the received radio ellite tag, and tag attachment type, ranged from 504 to transmissions through a radio receiver and a three-ele- 652 g. ment folding Yagi antenna (Advanced Telemetry Systems Because the purpose was to have tags remain attached Inc.; Isanti, MN, USA) to locate and recover the tag. on whales for days to weeks, recovery could be logistically difficult, especially if the animals vacated the area. Two Sample collection recovery aids were attached onto the TDR with zip ties. Tag testing occurred from August 2013 to October 2015 One was a satellite tag (SPOT-258A, Wildlife Computers; in a number of locations off California, including Bodega, Szesciorka et al. Anim Biotelemetry (2016) 4:18 Page 5 of 12 Table 1 Dimensions of tag attachment materials for individual suction cup and dart materials Individual tag attachment Cup diameter Dart length Dart stem Max width Weight of tag Material materials (mm) (mm) width (mm) of dart tip (mm) attachment (g) Suction cup (rigid) 77.8 – – – 68.0 Rubber Suction cup (semirigid) 80.9 – – – 56.7 Silicone Titanium—short 3-petal dart – 45.0 3.2 6.4 4.0 Grade 4 titanium Titanium—long 6-petal dart – 68.0 3.2 6.4 6.0 Grade 4 titanium Stainless steel—short conical dart – 17.5 3.2 5.6 17.0 17-4 PH stainless steel Stainless steel—long conical dart – 76.2 5.0 11.1 12.0 17-4 PH stainless steel Stainless steel—triangular dart – 76.2 5.0 9.8 11.3 17-4 PH stainless steel Stainless steel—long 3-petal dart – 80.0 5.0 6.0 10.0 17-4 PH stainless steel Stainless steel—long 6-petal dart – 80.0 5.0 6.0 11.0 17-4 PH stainless steel Half Moon Bay, Monterey Bay, and in the Santa Barbara they sloughed onto the suction cup tags or were removed Channel. Field operations were conducted using two when the darts detached from the animal, and used for rigid-hull inflatable boats. The tagging boat approached the purpose of sex identification. Photographs taken by whales to a range of a few meters and deployed the tags whale watch operators during the tagging years also were with a 3–5-m pole. The secondary boat searched for examined for additional tag site follow-ups. whales and provided safety support during tagging. Once a tag was deployed, the reaction of the animal Data analysis to tagging was noted. Each tagging event also was video Durations of tag attachment were determined from each recorded. If available, the videos and notes were reviewed dive record with Instrument Helper (Wildlife Comput- to score the reactions to tagging from 1 to 5 (based on ers; Redmond, WA, USA). Because sample sizes for the increasing severity of reaction) as: (1) no reaction, (2) tag attachment configurations were small and not always shallow dip dive, (3) slow dive or slight tail flick, (4) quick replicated between species, tag attachment configura - acceleration or dive, and (5) hard tail flick. While some tions were combined into broader groups for statistical whales exhibited multiple reactions, only the strongest analysis and species were analyzed separately. Humpback reaction was selected for each tagging event. whale tag attachment configurations were grouped as Photographs of each animal and tag were obtained with suction cup, suction cup with barb, two-dart (with pet- an EOS 7D digital single-lens reflex camera and 70–200- als), four-dart (no petals), and four-dart (with petals). mm telephoto zoom lens (Canon; Melville, NY, USA). Blue whale tag attachment configurations were grouped Fluke and dorsal photographs were used for follow-up as suction cup, four-dart (no petals), and four-dart (with monitoring and individual identification based on pig - petals). Due to small sample sizes and because the data mentation and markings on the underside of the flukes of violated assumptions necessary for parametric statistics, humpback whales [23] and on the right and left sides of we used one-way permutational analysis of variances blue whales [24]. For dart-attached tags where adequate (PERMANOVAs) to test for differences in tag attachment photographs were available, tag placement was scored duration and reaction to tagging by tag type for each spe- from 1 to 3 (based on how flush the tag was on the ani - cies. First, we calculated traditional F-statistics on the mal) as: (1) completely flush, (2) almost flush, and (3) not group means with the built-in ‘stats’ package in R [25]. fully attached. After a tag detached from the animal, the Then, we resampled the data 100,000 times with replace - tag floated to the surface and was retrieved after being ment using the built-in ‘base’ package in R and calculated located using the satellite tag data and VHF receiving a new F-statistic for each iteration. Lastly, we calculated gear. Photographs of each tag were taken upon recovery the probability of obtaining a new F-statistic as large as to assess any damage done to the tag or tag attachment our original F-statistic to test if there was an effect of tag system, including petal or dart breakage or bending. attachment type on tag attachment duration and reaction Recovery time and location also was noted. to tagging. Post hoc analysis was done with 100,000 pair- If possible, each animal was followed or re-sighted in wise permutational t tests with the ‘pairwise.perm.t.test’ successive days to photograph the status of the tag on function from the ‘RVAideMemoire’ package [26] in R. the animal or the tag site after the tag detached from the To account for Type I errors introduced by multiple pair- animal. Skin and blubber samples were collected, after wise tests and Type II errors introduced by small sample Szesciorka et al. Anim Biotelemetry (2016) 4:18 Page 6 of 12 Fig. 2 Titanium and stainless steel darts tested. a Short 3-petal titanium darts with petals clipped and rounded, b long 6-petal titanium darts with petals clipped and rounded, c short conical stainless steel dart used with suction cup, d long conical stainless steel dart, e triangular stainless steel dart, f long 6-petal stainless steel dart, and g long 3-petal stainless steel dart sizes, we applied the Benjamini and Hochberg False Dis- Results covery Rate correction [27] and set statistical significance From 2013 to 2015, 31 humpback whales and 20 blue at P  =  0.05. If available, follow-up photographs of tag whales were tagged with 10 tag attachment configu - attachment sites were analyzed qualitatively to note the rations. Tag attachment durations ranged from 0.0 to healing progress. 393.6  h, and all tag attachment configurations resulted Szesciorka et al. Anim Biotelemetry (2016) 4:18 Page 7 of 12 in greater median deployment durations on blue whales and 31 petals (14  %) lost, whereas of the nine deploy- (Table 2). ments with stainless steel darts with petals, tags were In three instances, tags deployed with semirigid suc- recovered with 1 dart (3  %) lost and 2 petals (1  %) lost tion cups with short conical stainless steel darts (n  =  2) (Table 3). Photographs of the stainless steel dart-attached and long conical stainless steel darts (n  =  1) penetrated tag while still attached to the whale indicated the dart the skin, but did not embed into the blubber layer, pull- came unscrewed from the carbon fiber plate outside of ing out immediately. In three additional instances, tags the whale, allowing it to rotate and eventually completely deployed with stainless steel triangular darts remained detach from the tag. Because we were not able to re- attached for less 1.5  h. To minimize unnecessary harm sight the two animals that had a titanium dart lost from and wasted effort, additional tests with these tag attach - the tags, we do not know whether the darts remained ment types were not pursued further; however, durations implanted in the animals; however, there no remnant for these deployments were included the analyses. pieces remained threaded in the carbon fiber plate to On four occasions, a tag broke on impact as the tags indicate dart breakage. The percentage of all recovered were being attached to animals. Two occurred with darts with one or more petals lost did not differ by spe - darted suction cups housed in syntactic foam, which cies (22 % humpback and 23 % blue whales). broke during tag deployment. Both tags were recovered. Most (81  %) tags were recovered within 24  h after the The other two instances involved tags with four stain - tag detached from the animal. On five occasions, we less steel darts. In these cases, the syntactic foam broke moved to another region to tag whales and returned in half due to the force of the pole and tag attachment within 33 and 84  h to retrieve the tags. On four occa- holder on the tag. One of the tags was lost, but in the sions, blue whales tagged in the southern California Bight other case, the carbon fiber plate held the tag together traveled 193–1031 km to the Baja California Peninsula in until it was retrieved. Durations for these deployments Mexico before the tags detached. Recovery of those tags were also included the analyses. was a priority because of the value of the tags, both in the Durations of tag attachment differed by tag attach - cost of the material and in the added value of weeks of ment type for humpback whales [PERMANOVA, dive data. In these instances, additional time for recov- F(4,26)  =  5.33, P  =  0.007] and blue whales [PER- ery was needed (1.17–18  days) for logistical planning, MANOVA, F(2,17)  =  59.63, P  =  0.006], rejecting the including chartering boats and waiting for safe weather, null hypothesis that all tag attachment types had equal especially following a hurricane in 2015. More than attachment durations. Post hoc analysis using pairwise half (67  %) of the recovered tags yielded skin and blub- permutational t tests indicated that durations of tag ber samples upon retrieval—18 samples from humpback attachment resulting from four-dart configurations with whales and 16 samples from blue whales. petals were significantly greater than suction cup tags for Three humpback whales were successfully re-sighted humpback whales (P  =  0.04; Fig.  3). Durations from all in Monterey Bay, CA, USA, and photographed 1–34 days tag attachments differed for blue whales (P < 0.04; Fig.  3). after the tag attachment failed and the tag detached Median tag attachment durations were greatest for four- (Fig.  4). Visual assessments and analysis of photographs dart configurations with petals for humpback whales indicated no evidence of external tearing or swelling at [30  h, interquartile range (IQR)  =  4.5–45.0  h] and blue the at the tag attachment site. whales (187  h, IQR  =  69.4–329.8  h; Fig.  3). There was no significant difference in reaction to tagging by tag Discussion attachment type for humpback whales [PERMANOVA, We found that tags attached with four-dart configura - F(4,23) = 1.65, P = 0.19] or blue whales (PERMANOVA, tions with petals resulted in the greatest attachment F(2,17) =  1.38, P = 0.24]. Although unbalanced tag test- durations with no difference in reaction to tagging by ing did not allow for a comparison of reaction to tagging tag type or by species. The switch to heat-treated stain - by species, humpback whales typically displayed stronger less steel darts reduced the incidence of petal breakage, reactions than blue whales (Table  2). Sample sizes were likely a combination of using a stronger material and too small for statistical analysis of the effect of tag place - heat-treating to increase material resilience. However, tag ment quality on tag attachment duration; however, there attachment duration also could be influenced by a num - was no clear pattern, with one of the greater durations ber of additional factors, including tag location, quality resulting from a tag not fully attached and some of the of placement, and behavioral differences in species and lesser durations resulting from tags that were completely individuals. flush with the animal (Table 2). The tags were attached as high up on the animals as Of the 12 deployments with titanium darts with petals, possible to maximize satellite and VHF transmission tags were recovered with a total of two darts (5  %) lost time when the animals came to the surface. However, Szesciorka et al. Anim Biotelemetry (2016) 4:18 Page 8 of 12 Table 2 Summary of  tag attachment durations for  10 tag attachment configurations for  humpback whales (Megaptera novaeangliae) and  blue whales (Balae - noptera musculus), grouped for statistical analysis as suction cup, suction cup with dart, two darts with petals, four darts (without petals), and four darts (with petals) Tag configurations Humpback whales Blue whales N Median Duration Reaction bins Placement N Median Duration Reaction bins Placement duration (h) range (h) scores duration (h) range (h) scores Suction cup (rigid) 11 3.40 0.32–6.82 2, 2, 2, 3, 3, 4, 4, – 10 10.86 0.33–24.25 1, 1, 1, 1, 2, 2, 2, – 5, 5, 5 2, 2, 4 Suction cup (semirigid) with short 4 0.38 0.00–2.54 1, 2, 2 – stainless steel dart Darts—two with petals Titanium—two short 3-petals darts 2 4.73 1.47–8.00 2, 5 1, 1 Titanium—two long 6-petal darts 1 – 6.92 5 2 Darts—four without petals Stainless steel—four conical darts 1 – 0.00 3 – 1 – 0.25 2 2 Stainless steel—four triangular barbs 2 0.95 0.65–1.25 2 2, 2 1 – 0.03 2 3 Darts—four with petals Titanium—two long 6-petal/two short 1 – 64.52 2 2 3 115.21 75.38–308.95 2, 2, 2 1, 2, 3 3-petal darts Titanium—four long 6-petal darts 4 10.04 0.02–49.92 4, 4, 4, 5 1, 2, 3 1 – 393.60 2 2 Stainless steel—four long 3-petal darts 2 40.93 40.23–41.63 1, 3 1, 2 1 – 51.58 4 1 Stainless steel—four long 6-petal darts 3 10.26 2.63–46.24 2, 5, 5 1, 2, 3 3 259.21 38.13–392.40 2, 2, 4 1, 2, 2 See “Methods”: Sample Collection for Reaction Bins and Placement Scores scoring definitions Three tagging events were unable to be scored. Total numbers in reaction bins do not match sample size Two tagging events could not be scored for placement. Total numbers in placement scores do not match sample size Szesciorka et al. Anim Biotelemetry (2016) 4:18 Page 9 of 12 Fig. 3 Box plots showing median tag attachment durations by tag type with first and third quartiles. a Humpback whale (Megaptera novaeangliae) tag configurations (left) were grouped as suction cup, suction cup with dart, two darts (with petals), four darts (no petals), and four darts (with pet - als). b Blue whale (Balaenoptera musculus) tag configurations (right) were grouped as suction cup, four darts (no petals), and four darts (with petals). Statistical differences from permutational pairwise t test, corrected with the Benjamini and Hochberg false discovery rate, are denoted by different letters Table 3 Outcome of  tags attached with  two or four darts The tag at its ultimate location will then be subject to titanium or stainless steel darts, including number of tags, drag forces as the animal moves through the water, and darts, and petals deployed and number (percent) lost depending on the tag attachment type and quality of the placement, this could further influence tag attachment Titanium Stainless steel duration [29]. Tag attachment configurations with two Deployed Lost (%) Deployed Lost (%) or more darts all need to penetrate the skin in order to Tags (2 or 4 darts 12 0 (0 %) 9 0 (0 %) be flush with the animal. If the tag is not fully flush, the with petals) tag also will likely be pulled out faster due to drag forces Darts 42 2 (5 %) 36 1 (3 %) and the animal’s movement. A number of short-duration Petals 216 31 (14 %) 180 2 (1 %) tag events were attributed to tags not being flush with the animal. However, some of the greater tag attachment durations resulted from tags that were not flush with the animals. Follow-up photographs of these tags on the ani- mals showed the tags becoming more flush with the ani - the location for tag placement was influenced by tag- mals over time, potentially due to water flow or contact ging conditions such as the boat driver and tagger, sea with other animals. conditions, and ease of placement, which varies by Finally, a difference in foraging strategies of tagged individual and species. For example, when blue whales animals could also play a role in tag attachment dura- surface, there is more surface area, allowing them to tion. Whereas blue whales feed almost exclusively on be tagged on the dorsal ridge just in front of the dorsal krill (euphausiid spp.; [30]), humpback whales exhibit fin. Humpback whales surface in a more arched posi- prey switching, feeding on dense concentrations of krill tion, typically only allowing for tag placement closer and schooling fish such as anchovy (Engraulis mordax), to the dorsal fin. Another determination factor for herring (Clupea spp.), sardine (Sardinops sagax), capelin tag placement, which has been studied in dolphins (Mallotus villosus) and sand lance (Ammodytes spp.; [e.g., but not yet for baleen whales, is selecting the ideal 31]). When feeding on fish, humpback whales tend to tag location based on tissue location, structure, and travel at greater speeds, make more exaggerated bending strength [28]. Szesciorka et al. Anim Biotelemetry (2016) 4:18 Page 10 of 12 Fig. 4 Photographic follow-ups with tagged whales. a Whale 20140601-6 tagged with two short (3 petals) titanium darts and again 2 and 34 days after tagging. b Whale 20140603-6 tagged with two long (6 petals) titanium darts and again 4 and 24 days after tagging. c Whale 20140604-5 tagged with two short (3 petals) and two long (6 petals) titanium darts and again 5 days after tagging and flexing movements, and usually feed in groups where and dove quickly. Mate et  al. [13] noted the reactions of whale-to-whale contact is common [32, 33]. Surface seven species of large whale to tagging, including reac- feeding can create additional drag forces from 2.5 to 5 tions as mild as head and fluke lifts, to evasive swimming times greater than animals at depth [34, 35]. Although we behavior, quick dives, and fluke swishes. In these other did not quantify prey during tagging, we observed tagged studies, the researchers noted that the responses to tag- humpback whales feeding on fish. These differences in ging were short-term, as was the case with this study. behavior due to foraging strategy could have influenced There have been few studies documenting healing fol - the duration that tags remained on humpback whales lowing tagging of large whales, especially with LIM- compared with duration on blue whales. PET and similarly designed darts. In developing early Response of animals to tagging with dart-attached tags implantable radio tags, Watkins et al. [12] found no signs did not elicit responses stronger than tagging with suc- of infection or tissue reaction at four tag-related wound tion cup-attached tags. Reactions ranged from no reac- sites 16–18  days post-attachment for humpback or fin tion to a hard tail flick. The range of reactions noted in whales. Mate et  al. [13] found that 40 re-sighted whales this study are consistent with the variability in reactions tagged between 1990 and 2005 exhibited varying levels of found within and among other species in a number of swelling or scarring at the tag site from implantable satel- previous studies [3, 36–39]. For example, Hooker et  al. lite tags; however, none were in poor health or showed [38] found no difference in observed response to tag signs of tissue sloughing at the tag site. Gendron et  al. deployments compared with biopsy sampling of north- [40] found extended periods of swelling when portions ern bottlenose whales (Hyperoodon ampullatus) and that of implantable tags remained embedded in tagged blue the behavioral state of the animal influenced the magni - whales. Best et  al. [41] reported scarring, but no swell- tude of the reaction. Watkins [39] noted that fin whales ing or difference in calving rates in re-sighted south - showed no reaction or moved away after being tagged; ern right whales (Eubalaena australis) that were tagged humpback whales had no reaction, swam faster, or fluked with implantable satellite tags. Similar to these studies, Szesciorka et al. Anim Biotelemetry (2016) 4:18 Page 11 of 12 Authors’ contributions follow-up photography of the site of tag attachment on AS, JC, and JH were involved in conception, study design, data collection and humpback whales up to 34  days after tagging indicated interpretation of the findings. AS collected and analyzed the data and was that the wounds exhibited no sign of tearing or swell- involved in laboratory analyses. AS, JC, and JH prepared the manuscript. All authors read and approved the final manuscript. ing, suggesting the modified darts had minimal physical impacts to the whales. Author details The four-dart configurations used in this study cre - Moss Landing Marine Laboratories, 8272 Moss Landing Rd, Moss Landing, CA 95039, USA. Cascadia Research Collective, 218 1/2 4th Ave W, Olympia, WA ated additional penetration points, each with the poten- 98501, USA. tial to allow for bacterial transfer inside the body [42]. However, the darts were small in width and length, Acknowledgements We thank Bill Watson and Kris Machado (MLML), for initial developments of tag thus limiting the depth of penetration into the blubber. attachment devices tested in this study. Thank you also to American Bench- Had the darts extended into the axial muscle, similar to mark Machine Works, especially Steve Jacobson and Jesse Brown, for creating implantable satellite tags, they would have been subject stainless steel barbs and plates for the tags. We also want to acknowledge Russ Andrews and Greg Schorr for ideas and discussions on dart design. Thank to the internal shearing forces between the blubber and you to the many volunteers that helped with tagging, especially James Fahl- muscle layers, creating deeper wounds in the blubber busch for his vital assistance in the field, Alison Stimpert for field assistance [40, 43]. and manuscript edits, Robin Baird for manuscript edits, and Nathan Harrison for assisting in some of the tag preparations. The tags also presented an opportunity to collect tis - sue samples. Although this is not a replacement for tradi- Competing interests tional biopsy methods, the collection of skin and blubber The authors declare that they have no competing interests. from suction cups and darts after the tags detached Availability of data and materials allowed us to lessen our physical contact with tagged The datasets analyzed during the current study are available from the cor- whales by not using traditional biopsy methods for this responding author on reasonable request. study. Tags retrieved up to 18 days after release from the Ethics approval and consent to participate animal yielded tissue samples that are being analyzed by All procedures performed were in accordance with the ethical standards Southwest Fisheries Science Center for the purpose of under MLML’s and Cascadia Research’s Institutional Animal Care and Use Committee protocols (#937 and #AUP-6, respectively), MLML’s and Cascadia sex identification. Research’s National Marine Fisheries Service Authorizations and Permits for Protected Species (#15271 and #16111, respectively), and MLML’s National Conclusions Oceanic and Atmospheric Administration Office of National Marine Sanctuar - ies multi-sanctuary research permit (#MULTI-2013-006). This study tested various tag attachment configurations to increase deployment duration of archival tags on large Funding whales while minimizing potential physical impacts to This research was funded by the Office of Naval Research [Grant No. N00014- 13-1-0772 to JC and Grant No. N00014-09-1-0632 to JH]. Additional funding whales. Tags with four-dart configurations with petals came from the American Cetacean Society, San Francisco Chapter; American resulted in the longest attachment durations on hump- Cetacean Society, Monterey Bay Chapter; California State University Council back and blue whales. The switch to heat-treated stain - on Ocean Affairs, Science and Technology; Dr. Earl Myers and Ethel M. Myers Oceanographic and Marine Biology Trust; California Professional Employer less steel allowed for the same tag attachment durations Organization; San Jose State University; David and Lucile Packard Foundation; as titanium, but with reduced dart or petal breakage. and Moss Landing Marine Laboratories [to AS]. Follow-ups with three tagged humpback whales indi- Received: 13 April 2016 Accepted: 1 September 2016 cated that the dart-attached tags created small wounds that showed no sign of tearing or swelling up to 34 days after tags detached. The use of dart-attached archival tags has presented new opportunities to collect high- resolution data over intermediate (weeks) time periods. References Although archival tags need to be recovered, these tags 1. Scholander P. Experimental investigations on the respiratory function in diving mammals and birds. Hvalradets Skrifter. 1940;22:1–131. can include a suite of high-sampling kinematic, acous- 2. Kooyman GL. Genesis and evolution of bio-logging devices: 1963–2002. tic, and environmental sensors. Using intermediate-term Mem Natl Inst Polar Res Ser. 2004;58:15–22. dart-attached archival tags, we can answer questions 3. Johnson M. Aguilar de Soto N, Madsen PT. Studying the behaviour and sensory ecology of marine mammals using acoustic recording tags: a about foraging efficiency, daily diving and transit activity, review. Mar Ecol Prog Ser. 2009;395:55–77. and diel trends. 4. Hazen EL, Maxwell SM, Bailey H, Bograd SJ, Hamann M, Gaspar P, Godley BJ, Shillinger GL. Ontogeny in marine tagging and tracking science: technologies and data gaps. Mar Ecol Prog Ser. 2012;457:221–40. Abbreviations 5. Goldbogen JA, Friedlaender AS, Calambokidis J, McKenna MF, Simon ARGOS: Advanced Research and Global Observation Satellite; C: celsius; GPS: M, Nowacek DP. Integrative approaches to the study of baleen whale global positioning system; LIMPET: low impact minimally percutaneous diving behavior, feeding performance, and foraging ecology. Bioscience. external-electronics transmitter; MLML: Moss Landing Marine Laboratories; 2013;63:90–100. SPOT: SPOT-257A satellite tag; TDR: time-depth recorder; VHF: very high 6. Norris KS, Evans WE, Ray GC. New tagging and tracking methods for the frequency. study of marine mammal biology and migration. In: Shevill WE, editor. Szesciorka et al. Anim Biotelemetry (2016) 4:18 Page 12 of 12 The whale problem: a status report. Cambridge: Harvard University Press; 27. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a 1974. practical and powerful approach to multiple testing. J R Stat Soc B. 7. Frost KJ, Lowry LF, Nelson RR. Radiotagging studies of belukha 1995;57:289–300. whales (Delphinapterus leucas) in Bristol Bay. Alaska Mar Mamm Sci. 28. Andrews RD, Baird RW, Schorr GS, Mittal R, Howle LE, Hanson MB. 1985;1:191–202. Improving attachments of remotely-deployed dorsal fin-mounted tags: 8. Scott MD, Wells RS, Irvine AB, Mate BR. Tagging and marking studies on tissue structure, hydrodynamics, in situ performance, and tagged-animal small cetaceans. In: Leatherwood S, Reeves RR, editors. The bottlenose follow-up. Seattle: Office of Naval Research; 2015. ONR Report Award dolphin. San Diego: Academic Press; 1990. Number: N000141010686. 9. Jeffries SJ, Brown RF, Harvey JT. Techniques for capturing, handling and 29. Shorter KA, Murray MM, Johnson M, Moore M, Howle LE. Drag of suc- marking harbour seals. Aquat Mamm. 1993;19:21–5. tion cup tags on swimming animals: modeling and measurement. Mar 10. Burgess WC, Tyack PL, Le Boeuf BJ, Costa DP. A programmable acoustic Mamm Sci. 2014;30:726–46. recording tag and first results from free-ranging northern elephant seals. 30. Croll DA, Tershy BR, Hewitt RP, Demer DA, Fiedler PC, Smith SE, Armstrong Deep-Sea Res Part II. 1998;45(7):1327–51. W, Popp JM, Kiekhefer T, Lopez VR, Urban J, Gendron D. An integrated 11. Fossette S, Ferraroli S, Tanaka H, Ropert-Coudert Y, Arai N, Sato K, Naito Y, approach to the foraging ecology of marine birds and mammals. Deep- Le Maho Y, Georges JY. Dispersal and dive patterns in gravid leatherback Sea Res Pt II. 1998;45:1353–71. turtles during the nesting season in French Guiana. Mar Ecol Prog Ser. 31. Wiley D, Ware C, Bocconcelli A, Cholewiak D, Friedlaender AS, Thompson 2007;338:233–47. M, Weinrich M. Underwater components of humpback whale bubble-net 12. Watkins WA, Schevill WE. The development and testing of a radio whale feeding behaviour. Behaviour. 2011;148(5–6):575–602. tag. Woods Hole: Woods Hole Oceanographic Institution; 1977. 32. Ware C, Friedlaender AS, Nowacek DP. Shallow and deep lunge feeding of 13. Mate B, Mesecar R, Lagerquist B. The evolution of satellite-monitored humpback whales in fjords of the West Antarctic Peninsula. Mar Mamm radio tags for large whales: one laboratory’s experience. Deep-Sea Res Sci. 2011;27(3):587–605. Part II. 2007;54(3–4):224–47. 33. Simon M, Johnson M, Madsen PT. Keeping momentum with a mouthful 14. Mate BR, Krutzikowsky GK, Winson MH. Satellite-monitored movements of water: behavior and kinematics of humpback whale lunge feeding. J of radio-tagged bowhead whales in the Beaufort and Chukchi seas Exp Biol. 2012;215:3786–98. during the late-summer feeding season and fall migration. Can J Zool. 34. Blake RW. Biological implications of the hydrodynamics of swimming at 2000;78:1168–81. or near the surface and in shallow water. Bioinspir Biomim. 2009;4:1–9. 15. Lagerquist BA, Mate BR, Ortega-Ortiz JG, Winsor M, Urban-Ramirez 35. Goldman JA. Eec ff ts of the free water surface on animals that jump out of J. Migratory movements and surfacing rates of humpback whales the water. Ph.D. thesis, Duke University, Durham, NC; 2001. (Megaptera novaeangliae) satellite tagged at Socorro Island, Mexico. Mar 36. Schneider K, Baird RW, Dawson S, Visser I, Childerhouse S. Reactions of Mamm Sci. 2008;24:815–30. bottlenose dolphins to tagging attempts using a remotely-deployed 16. Hooker SK, Baird RW. Diving and ranging behaviour of odontocetes: a suction-cup tag. Mar Mamm Sci. 1998;14:316–24. methodological review and critique. Mamm Rev. 2001;31(1):81–105. 37. Stimpert AK, Matilla D, Nosal E, Whitlow WLA. Tagging young humpback 17. Schorr GS, Falcone EA, Moretti DJ, Andrews RD. First long-term behavioral whale calves: methodology and diving behavior. Endanger Spec Res. records from Cuvier’s Beaked Whales (Ziphius cavirostris) reveal record- 2012;19:11–7. breaking dives. PLoS One. 2014. doi:10.1371/journal.pone.0092633. 38. Hooker SK, Baird RW, Al-Omari S, Gowans S, Whitehead H. Behavioral 18. Goodyear J. A new radio tag; the Remora, and behavior of a humpback reactions of northern bottlenose whales (Hyperoodon ampullatus) to whale (Megaptera novaeangliae). J Cetacean Res. 1981;2:1–2. biopsy darting and tag attachment procedures Fish. Bull. 2001;99:303–8. 19. Baird RW. Studying diving behavior of whales and dolphins using suc- 39. Watkins WA. Reaction of three species of whales Balaenoptera physalus, tion-cup attached tags. Whalewatcher: J Am Cetac Soc. 1998;31(1):3–7. Megaptera novaeangliae, and Balaenoptera edeni to implanted radio tags. 20. Andrews RD, Pitman RL, Ballance LT. Satellite tracking reveals distinct Deep-Sea Res. 1981;28(6):589–99. movement patterns for Type B and Type C killer whales in the southern 40. Gendron D, Martinez Serrano I, Ugalde de la Cruz A, Calambokidis J, Ross Sea, Antarctica. Polar Biol. 2008;31:1461–8. Mate B. Long-term individual sighting history database: an effective 21. Andrews RD. Improving attachments of remotely-deployed dorsal fin- tool to monitor satellite tag effects on cetaceans. Endang Species Res. mounted tags: tissue structure, hydrodynamics, in situ performance, and 2015;26:235–41. tagged-animal follow-up. Seattle: Office of Naval Research; 2011. ONR 41. Best PB, Mate B, Lagerquist B. Tag retention, wound healing, and subse- Report Award Number: N000141010686. quent reproductive history of southern right whales following satellite- 22. Clapham PJ. Humpback Whales. Stillwater: Voyageur Press; 1996. tagging. Mar Mamm Sci. 2015;31:520–39. 23. Katona S, Baxter SB, Brazier O, Kraus S, Perkins J, Whitehead H. Identifica- 42. Weller DW. Report of the large whale tagging workshop. San Diego: U.S. tion of humpback whales by fluke photographs. In: Winn HW, Olla BL, edi- Marine Mammal Commission; 2008. tors. Behavior of marine animals. Volume 3. Cetaceans. New York: Plenum 43. Moore M, Andrews R, Austin T, Bailey J, Costidis A, George C, Jackson K, Press; 1979. Pitchford T, Landry S, Ligon A, McLellan W, Morin D, Smith J, Rotstein D, 24. Sears R. The photographic identification of individual blue whales Balae - Rowles T, Slay C, Walsh M. Rope trauma, sedation, disentanglement, and noptera musculus in the Sea of Cortez. Cetus. 1987;7(1):14–7. monitoring-tag associated lesions in a terminally entangled North Atlan- 25. R Core Team. R: A language and environment for statistical computing. tic right whale (Eubalaena glacialis). Mar Mamm Sci. 2013;29:E98–113. R Foundation for Statistical Computing, Vienna, Austria. 2016; https:// www.R-project.org/. 26. Maxime Hervé. RVAideMemoire: Diverse Basic Statistical and Graphical Functions. R package version 0.9-55. 2016; https://CRAN.R-project.org/ package=RVAideMemoire. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Animal Biotelemetry Springer Journals

Testing tag attachments to increase the attachment duration of archival tags on baleen whales

Loading next page...
 
/lp/springer-journals/testing-tag-attachments-to-increase-the-attachment-duration-of-QuxeQa1lvc
Publisher
Springer Journals
Copyright
Copyright © 2016 by The Author(s)
Subject
Life Sciences; Animal Systematics/Taxonomy/Biogeography; Conservation Biology/Ecology; Terrestial Ecology; Bioinformatics; Freshwater & Marine Ecology
eISSN
2050-3385
DOI
10.1186/s40317-016-0110-y
Publisher site
See Article on Publisher Site

Abstract

Background: As biologging technology has advanced to study whale behavior, various tag attachment methods have been developed. Suction cup attachments were developed for short-term (<24 h) studies using high-resolution archival tags, and implantable or dart attachments were developed for long-term (months) studies using coarse- resolution satellite tags. The purpose of this study was to test various tag attachment configurations to increase the deployment duration of archival tags while minimizing potential physical impacts to the whale. Results: From 2013 to 2015, 31 humpback whales (Megaptera novaeangliae) and 20 blue whales (Balaenoptera mus- culus) were tagged, allowing us to test 10 tag attachment configurations, grouped as suction cup, suction cup with dart, two-dart configurations with petals, four-dart configurations, and four-dart configurations with petals. Dura- tions resulting from four-dart configurations with petals were greater than suction cup tags for humpback whales (P = 0.04). Durations resulting from four-dart configurations with petals were greater than all other tag attachment types for blue whales (P < 0.04). There was no difference in reaction to tagging by tag attachment type for humpback (P = 0.19) or blue whales (P = 0.24). Tags attached with titanium darts were recovered with 2 darts (5 %) lost and 31 petals (14 %) broken, whereas tags attached with stainless steel darts were recovered with 1 dart (3 %) lost and 2 petals (1 %) broken. Re-sights of three tagged animals up to 34 days after tags detached showed no sign of tearing or swelling at the tag site. Conclusions: Tag attachments using four darts with petals remained on whales the longest with no increase in reac- tion to tagging by either species. Heat-treated stainless steel darts resulted in equivalent tag attachment durations as titanium darts but with reduced petal breakage. Attachments with four darts, despite creating additional points of entry for potential bacterial transfer, did not produce signs of tearing or swelling on animals re-sighted up to 34 days after tagging. Attaching archival tags with four stainless steel darts with petals on baleen whales will allow for the collection of weeks of fine-scale data, allowing researchers to answer questions about foraging, daily activity, and diel trends. Keywords: Biologging, Long-term tag, Tag development, Baleen whale, Dive behavior technology has quickly advanced, integrating GPS, accel- Background erometers, magnetometers, pressure sensors, and acous- The first measurement of the maximum dive depth of a tic recorders that allow for the collection of biological, marine animal was recorded when a capillary-tube pres- environmental, and behavioral information on free rang- sure gauge was attached to a fin whale ( Balaenoptera ing marine animals [2–5]. physalus) with a harpoon [1]. Since then, biologging As new tag technology was being introduced, so were methods of tag attachment. Unlike turtles, pinnipeds, *Correspondence: angela@szesciorka.com and small odontocetes that could be captured and tagged Moss Landing Marine Laboratories, 8272 Moss Landing Rd, Moss using harnesses, rings, epoxies, and acrylic glues [e.g., Landing, CA 95039, USA Full list of author information is available at the end of the article © 2016 The Author(s). This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Szesciorka et al. Anim Biotelemetry (2016) 4:18 Page 3 of 12 6–11], large whales could not be captured and their The short 3-petal and long 6-petal Grade 4 titanium smooth, hairless, and regularly sloughed skin made epoxy darts (Fig.  2a, b) were manufactured by Wildlife Com- or glue methods impossible. This led to the development puters (Redmond, WA, USA) for the Low Impact Mini- of tag attachments that could be implanted into the bod- mally Percutaneous External-electronics Transmitter ies of larger cetaceans using modified crossbows or pneu - (LIMPET) system, based on designs developed by Russ matic guns [12, 13]. Andrews [20, 21]. Implantable tags were designed to pen- Implantable satellite tags allowed for long-term tag etrate the fascia and muscle layers of the whale, opening deployments (months) on whales, enabling researchers to up the possibility of bacterial transfer inside the body answer questions about distribution and movement [13– leading to inflammation and infection. To reduce poten - 15]. However, satellite transmissions can only send small tial physical impact on whales, the LIMPET darts do not amounts of compressed data at each uplink, which can exceed 8  cm in length so they do not penetrate beneath be affected by the number of satellites present at the time the blubber layer, which for humpback whales is ~15 cm of uplink and how long the animal remains at the surface deep [22], whereas implantable tags penetrate into the [16]. Using a combination of transmission to satellites blubber and into the muscle as deep as 30.5 cm [12, 13]. augmented with shore-receiving stations has allowed The backwards-facing petals of the titanium darts pro - some transmission of more detailed data [17]. Because vided anchoring when the tag penetrated the blubber bandwidth limitation results in coarse-resolution data, layer. For both long and short titanium darts, the pet- these tags are typically not suitable for fine-scale studies als were clipped to roughly two-thirds of their original of behavior. length and rounded to reduce potential tearing as the Another direction in tag attachment has been the use darts worked their way out of the animal. of suction cup-attached archival tags that do not pene- The short, conical, and triangular machinable certified trate the skin [18]. In addition to being readily available, 17-4 PH stainless steel darts were manufactured at Moss inexpensive, and easy to attach via crossbow or pole [19], Landing Marine Laboratories (Moss Landing, CA, USA; these tags were designed to collect data at high-sampling Fig.  2c–e). The long 3- and 6-petal machinable certified rates, allowing for the collection of fine-scale informa - 17-4 PH stainless darts (Fig. 2f, g) were manufactured by tion on behavior [16]. The tags needed to be recovered to American Benchmark Machine Works (Olympia, WA, retrieve the data, so they were not constrained by band- USA). These darts were designed to be similar to the width limits like satellite tags. However, because suc- titanium darts from the LIMPET system, but were con- tion cup-attached tags typically remained on for <24  h, structed using stainless steel, which is less brittle than researchers could not answer questions about fine-scale titanium. Welding petals onto the darts adds excess heat behavior at time scales of days to weeks. to the surface area of petals, creating weaknesses where The purpose of this study was to test various tag attach - breakage can occur. To decrease the risk of petal break- ment configurations, including methods typically used age from welding and lessen the effects of elongation with dart-attached satellite tags to increase the deploy- (how much the material stretches before breaking), the ment duration of archival tags, ultimately allowing for the darts were heat-treated at 1100 °F for 4 h. collection of high-resolution behavior data over interme- These tag attachment materials were tested in 10 con - diate time periods (days to weeks) compared with current figurations: (1) suction cup (rigid), (2) suction cup (semi - suction cup-attached archival tags (<24  h), while mini- rigid) with a short conical stainless steel dart, (3) two mizing the potential physical impacts to the whale. short (3 petals each) titanium darts, (4) two long (6 pet- als each) titanium darts, (5) four long stainless steel coni- Methods cal darts, (6) four stainless steel triangular darts, (7) two Tag attachment development short (3 petals each)/two long (six petals each) titanium The tag attachments tested in this study included vari - darts, (8) four long (6 petals each) titanium darts, (9) four ous configurations of suction cup (Fig.  1a), darted suc- long (3 petals each) stainless steel darts, and (10) four tion cup (Fig.  1b), two-dart configurations with petals long (6 petals each) stainless steel darts. To minimize (Fig. 1c), four-dart configurations (Fig.  1d), and four-dart bacterial transfer and risk of infection, the darts were gas configurations with petals (Fig.  1e). Individual tag attach- sterilized in ethylene oxide (Sequoia Veterinary Hospital; ment materials included two types of suction cup, two Redwood City, CA, USA), cleaned in 70 % rubbing alco- Grade 4 titanium darts, and five machinable certified hol, and coated with 7.5  % povidone-iodine (Betadine) 17-4 PH stainless steel darts (Table 1). surgical scrub solution before tagging. Rigid suction cups came from Canadian Tire (Toronto, The tag attachment methods were tested by attach - ON, USA; Fig. 1a), and semirigid suction cups came from ing a time-depth recorder (TDR) archival tag (Wildlife Cetacean Research Technology (Seattle, WA; Fig.  1b). Computers; Redmond, WA, USA) below the dorsal fin Szesciorka et al. Anim Biotelemetry (2016) 4:18 Page 4 of 12 Fig. 1 TDR tags with syntactic foam, radio transmitter and/or satellite tag, and tag attachment. a Suction cup attachment, b suction cup with dart attachment, c two darts with petals, d four darts with no petals, and e four darts with petals of humpback whales or on the dorsal ridge just forward Redmond, WA, USA), which weighed 53  g. The satel - the dorsal fin of blue whales. Tags were attached as high lite tag was programmed to transmit via the Argos sys- on each animal as possible to maximize reception of the tem, providing position estimates within 250 m when the satellite tag and VHF transmitter. The TDR’s dimensions tag was detached and floating at the water’s surface. The were 102  mm  ×  56  mm  ×  30  mm, and they weighed second recovery aid was a 10-g VHF transmitter (Series 225  g in air. The TDRs were glued into a syntactic foam MM100, Advanced Telemetry Systems Inc.; Isanti, MN, housing for floatation that varied in shape and weight. USA). Once within range of the tag’s last estimated posi- Total tag weight, including the syntactic foam, VHF, sat- tion, we used the pulse strength of the received radio ellite tag, and tag attachment type, ranged from 504 to transmissions through a radio receiver and a three-ele- 652 g. ment folding Yagi antenna (Advanced Telemetry Systems Because the purpose was to have tags remain attached Inc.; Isanti, MN, USA) to locate and recover the tag. on whales for days to weeks, recovery could be logistically difficult, especially if the animals vacated the area. Two Sample collection recovery aids were attached onto the TDR with zip ties. Tag testing occurred from August 2013 to October 2015 One was a satellite tag (SPOT-258A, Wildlife Computers; in a number of locations off California, including Bodega, Szesciorka et al. Anim Biotelemetry (2016) 4:18 Page 5 of 12 Table 1 Dimensions of tag attachment materials for individual suction cup and dart materials Individual tag attachment Cup diameter Dart length Dart stem Max width Weight of tag Material materials (mm) (mm) width (mm) of dart tip (mm) attachment (g) Suction cup (rigid) 77.8 – – – 68.0 Rubber Suction cup (semirigid) 80.9 – – – 56.7 Silicone Titanium—short 3-petal dart – 45.0 3.2 6.4 4.0 Grade 4 titanium Titanium—long 6-petal dart – 68.0 3.2 6.4 6.0 Grade 4 titanium Stainless steel—short conical dart – 17.5 3.2 5.6 17.0 17-4 PH stainless steel Stainless steel—long conical dart – 76.2 5.0 11.1 12.0 17-4 PH stainless steel Stainless steel—triangular dart – 76.2 5.0 9.8 11.3 17-4 PH stainless steel Stainless steel—long 3-petal dart – 80.0 5.0 6.0 10.0 17-4 PH stainless steel Stainless steel—long 6-petal dart – 80.0 5.0 6.0 11.0 17-4 PH stainless steel Half Moon Bay, Monterey Bay, and in the Santa Barbara they sloughed onto the suction cup tags or were removed Channel. Field operations were conducted using two when the darts detached from the animal, and used for rigid-hull inflatable boats. The tagging boat approached the purpose of sex identification. Photographs taken by whales to a range of a few meters and deployed the tags whale watch operators during the tagging years also were with a 3–5-m pole. The secondary boat searched for examined for additional tag site follow-ups. whales and provided safety support during tagging. Once a tag was deployed, the reaction of the animal Data analysis to tagging was noted. Each tagging event also was video Durations of tag attachment were determined from each recorded. If available, the videos and notes were reviewed dive record with Instrument Helper (Wildlife Comput- to score the reactions to tagging from 1 to 5 (based on ers; Redmond, WA, USA). Because sample sizes for the increasing severity of reaction) as: (1) no reaction, (2) tag attachment configurations were small and not always shallow dip dive, (3) slow dive or slight tail flick, (4) quick replicated between species, tag attachment configura - acceleration or dive, and (5) hard tail flick. While some tions were combined into broader groups for statistical whales exhibited multiple reactions, only the strongest analysis and species were analyzed separately. Humpback reaction was selected for each tagging event. whale tag attachment configurations were grouped as Photographs of each animal and tag were obtained with suction cup, suction cup with barb, two-dart (with pet- an EOS 7D digital single-lens reflex camera and 70–200- als), four-dart (no petals), and four-dart (with petals). mm telephoto zoom lens (Canon; Melville, NY, USA). Blue whale tag attachment configurations were grouped Fluke and dorsal photographs were used for follow-up as suction cup, four-dart (no petals), and four-dart (with monitoring and individual identification based on pig - petals). Due to small sample sizes and because the data mentation and markings on the underside of the flukes of violated assumptions necessary for parametric statistics, humpback whales [23] and on the right and left sides of we used one-way permutational analysis of variances blue whales [24]. For dart-attached tags where adequate (PERMANOVAs) to test for differences in tag attachment photographs were available, tag placement was scored duration and reaction to tagging by tag type for each spe- from 1 to 3 (based on how flush the tag was on the ani - cies. First, we calculated traditional F-statistics on the mal) as: (1) completely flush, (2) almost flush, and (3) not group means with the built-in ‘stats’ package in R [25]. fully attached. After a tag detached from the animal, the Then, we resampled the data 100,000 times with replace - tag floated to the surface and was retrieved after being ment using the built-in ‘base’ package in R and calculated located using the satellite tag data and VHF receiving a new F-statistic for each iteration. Lastly, we calculated gear. Photographs of each tag were taken upon recovery the probability of obtaining a new F-statistic as large as to assess any damage done to the tag or tag attachment our original F-statistic to test if there was an effect of tag system, including petal or dart breakage or bending. attachment type on tag attachment duration and reaction Recovery time and location also was noted. to tagging. Post hoc analysis was done with 100,000 pair- If possible, each animal was followed or re-sighted in wise permutational t tests with the ‘pairwise.perm.t.test’ successive days to photograph the status of the tag on function from the ‘RVAideMemoire’ package [26] in R. the animal or the tag site after the tag detached from the To account for Type I errors introduced by multiple pair- animal. Skin and blubber samples were collected, after wise tests and Type II errors introduced by small sample Szesciorka et al. Anim Biotelemetry (2016) 4:18 Page 6 of 12 Fig. 2 Titanium and stainless steel darts tested. a Short 3-petal titanium darts with petals clipped and rounded, b long 6-petal titanium darts with petals clipped and rounded, c short conical stainless steel dart used with suction cup, d long conical stainless steel dart, e triangular stainless steel dart, f long 6-petal stainless steel dart, and g long 3-petal stainless steel dart sizes, we applied the Benjamini and Hochberg False Dis- Results covery Rate correction [27] and set statistical significance From 2013 to 2015, 31 humpback whales and 20 blue at P  =  0.05. If available, follow-up photographs of tag whales were tagged with 10 tag attachment configu - attachment sites were analyzed qualitatively to note the rations. Tag attachment durations ranged from 0.0 to healing progress. 393.6  h, and all tag attachment configurations resulted Szesciorka et al. Anim Biotelemetry (2016) 4:18 Page 7 of 12 in greater median deployment durations on blue whales and 31 petals (14  %) lost, whereas of the nine deploy- (Table 2). ments with stainless steel darts with petals, tags were In three instances, tags deployed with semirigid suc- recovered with 1 dart (3  %) lost and 2 petals (1  %) lost tion cups with short conical stainless steel darts (n  =  2) (Table 3). Photographs of the stainless steel dart-attached and long conical stainless steel darts (n  =  1) penetrated tag while still attached to the whale indicated the dart the skin, but did not embed into the blubber layer, pull- came unscrewed from the carbon fiber plate outside of ing out immediately. In three additional instances, tags the whale, allowing it to rotate and eventually completely deployed with stainless steel triangular darts remained detach from the tag. Because we were not able to re- attached for less 1.5  h. To minimize unnecessary harm sight the two animals that had a titanium dart lost from and wasted effort, additional tests with these tag attach - the tags, we do not know whether the darts remained ment types were not pursued further; however, durations implanted in the animals; however, there no remnant for these deployments were included the analyses. pieces remained threaded in the carbon fiber plate to On four occasions, a tag broke on impact as the tags indicate dart breakage. The percentage of all recovered were being attached to animals. Two occurred with darts with one or more petals lost did not differ by spe - darted suction cups housed in syntactic foam, which cies (22 % humpback and 23 % blue whales). broke during tag deployment. Both tags were recovered. Most (81  %) tags were recovered within 24  h after the The other two instances involved tags with four stain - tag detached from the animal. On five occasions, we less steel darts. In these cases, the syntactic foam broke moved to another region to tag whales and returned in half due to the force of the pole and tag attachment within 33 and 84  h to retrieve the tags. On four occa- holder on the tag. One of the tags was lost, but in the sions, blue whales tagged in the southern California Bight other case, the carbon fiber plate held the tag together traveled 193–1031 km to the Baja California Peninsula in until it was retrieved. Durations for these deployments Mexico before the tags detached. Recovery of those tags were also included the analyses. was a priority because of the value of the tags, both in the Durations of tag attachment differed by tag attach - cost of the material and in the added value of weeks of ment type for humpback whales [PERMANOVA, dive data. In these instances, additional time for recov- F(4,26)  =  5.33, P  =  0.007] and blue whales [PER- ery was needed (1.17–18  days) for logistical planning, MANOVA, F(2,17)  =  59.63, P  =  0.006], rejecting the including chartering boats and waiting for safe weather, null hypothesis that all tag attachment types had equal especially following a hurricane in 2015. More than attachment durations. Post hoc analysis using pairwise half (67  %) of the recovered tags yielded skin and blub- permutational t tests indicated that durations of tag ber samples upon retrieval—18 samples from humpback attachment resulting from four-dart configurations with whales and 16 samples from blue whales. petals were significantly greater than suction cup tags for Three humpback whales were successfully re-sighted humpback whales (P  =  0.04; Fig.  3). Durations from all in Monterey Bay, CA, USA, and photographed 1–34 days tag attachments differed for blue whales (P < 0.04; Fig.  3). after the tag attachment failed and the tag detached Median tag attachment durations were greatest for four- (Fig.  4). Visual assessments and analysis of photographs dart configurations with petals for humpback whales indicated no evidence of external tearing or swelling at [30  h, interquartile range (IQR)  =  4.5–45.0  h] and blue the at the tag attachment site. whales (187  h, IQR  =  69.4–329.8  h; Fig.  3). There was no significant difference in reaction to tagging by tag Discussion attachment type for humpback whales [PERMANOVA, We found that tags attached with four-dart configura - F(4,23) = 1.65, P = 0.19] or blue whales (PERMANOVA, tions with petals resulted in the greatest attachment F(2,17) =  1.38, P = 0.24]. Although unbalanced tag test- durations with no difference in reaction to tagging by ing did not allow for a comparison of reaction to tagging tag type or by species. The switch to heat-treated stain - by species, humpback whales typically displayed stronger less steel darts reduced the incidence of petal breakage, reactions than blue whales (Table  2). Sample sizes were likely a combination of using a stronger material and too small for statistical analysis of the effect of tag place - heat-treating to increase material resilience. However, tag ment quality on tag attachment duration; however, there attachment duration also could be influenced by a num - was no clear pattern, with one of the greater durations ber of additional factors, including tag location, quality resulting from a tag not fully attached and some of the of placement, and behavioral differences in species and lesser durations resulting from tags that were completely individuals. flush with the animal (Table 2). The tags were attached as high up on the animals as Of the 12 deployments with titanium darts with petals, possible to maximize satellite and VHF transmission tags were recovered with a total of two darts (5  %) lost time when the animals came to the surface. However, Szesciorka et al. Anim Biotelemetry (2016) 4:18 Page 8 of 12 Table 2 Summary of  tag attachment durations for  10 tag attachment configurations for  humpback whales (Megaptera novaeangliae) and  blue whales (Balae - noptera musculus), grouped for statistical analysis as suction cup, suction cup with dart, two darts with petals, four darts (without petals), and four darts (with petals) Tag configurations Humpback whales Blue whales N Median Duration Reaction bins Placement N Median Duration Reaction bins Placement duration (h) range (h) scores duration (h) range (h) scores Suction cup (rigid) 11 3.40 0.32–6.82 2, 2, 2, 3, 3, 4, 4, – 10 10.86 0.33–24.25 1, 1, 1, 1, 2, 2, 2, – 5, 5, 5 2, 2, 4 Suction cup (semirigid) with short 4 0.38 0.00–2.54 1, 2, 2 – stainless steel dart Darts—two with petals Titanium—two short 3-petals darts 2 4.73 1.47–8.00 2, 5 1, 1 Titanium—two long 6-petal darts 1 – 6.92 5 2 Darts—four without petals Stainless steel—four conical darts 1 – 0.00 3 – 1 – 0.25 2 2 Stainless steel—four triangular barbs 2 0.95 0.65–1.25 2 2, 2 1 – 0.03 2 3 Darts—four with petals Titanium—two long 6-petal/two short 1 – 64.52 2 2 3 115.21 75.38–308.95 2, 2, 2 1, 2, 3 3-petal darts Titanium—four long 6-petal darts 4 10.04 0.02–49.92 4, 4, 4, 5 1, 2, 3 1 – 393.60 2 2 Stainless steel—four long 3-petal darts 2 40.93 40.23–41.63 1, 3 1, 2 1 – 51.58 4 1 Stainless steel—four long 6-petal darts 3 10.26 2.63–46.24 2, 5, 5 1, 2, 3 3 259.21 38.13–392.40 2, 2, 4 1, 2, 2 See “Methods”: Sample Collection for Reaction Bins and Placement Scores scoring definitions Three tagging events were unable to be scored. Total numbers in reaction bins do not match sample size Two tagging events could not be scored for placement. Total numbers in placement scores do not match sample size Szesciorka et al. Anim Biotelemetry (2016) 4:18 Page 9 of 12 Fig. 3 Box plots showing median tag attachment durations by tag type with first and third quartiles. a Humpback whale (Megaptera novaeangliae) tag configurations (left) were grouped as suction cup, suction cup with dart, two darts (with petals), four darts (no petals), and four darts (with pet - als). b Blue whale (Balaenoptera musculus) tag configurations (right) were grouped as suction cup, four darts (no petals), and four darts (with petals). Statistical differences from permutational pairwise t test, corrected with the Benjamini and Hochberg false discovery rate, are denoted by different letters Table 3 Outcome of  tags attached with  two or four darts The tag at its ultimate location will then be subject to titanium or stainless steel darts, including number of tags, drag forces as the animal moves through the water, and darts, and petals deployed and number (percent) lost depending on the tag attachment type and quality of the placement, this could further influence tag attachment Titanium Stainless steel duration [29]. Tag attachment configurations with two Deployed Lost (%) Deployed Lost (%) or more darts all need to penetrate the skin in order to Tags (2 or 4 darts 12 0 (0 %) 9 0 (0 %) be flush with the animal. If the tag is not fully flush, the with petals) tag also will likely be pulled out faster due to drag forces Darts 42 2 (5 %) 36 1 (3 %) and the animal’s movement. A number of short-duration Petals 216 31 (14 %) 180 2 (1 %) tag events were attributed to tags not being flush with the animal. However, some of the greater tag attachment durations resulted from tags that were not flush with the animals. Follow-up photographs of these tags on the ani- mals showed the tags becoming more flush with the ani - the location for tag placement was influenced by tag- mals over time, potentially due to water flow or contact ging conditions such as the boat driver and tagger, sea with other animals. conditions, and ease of placement, which varies by Finally, a difference in foraging strategies of tagged individual and species. For example, when blue whales animals could also play a role in tag attachment dura- surface, there is more surface area, allowing them to tion. Whereas blue whales feed almost exclusively on be tagged on the dorsal ridge just in front of the dorsal krill (euphausiid spp.; [30]), humpback whales exhibit fin. Humpback whales surface in a more arched posi- prey switching, feeding on dense concentrations of krill tion, typically only allowing for tag placement closer and schooling fish such as anchovy (Engraulis mordax), to the dorsal fin. Another determination factor for herring (Clupea spp.), sardine (Sardinops sagax), capelin tag placement, which has been studied in dolphins (Mallotus villosus) and sand lance (Ammodytes spp.; [e.g., but not yet for baleen whales, is selecting the ideal 31]). When feeding on fish, humpback whales tend to tag location based on tissue location, structure, and travel at greater speeds, make more exaggerated bending strength [28]. Szesciorka et al. Anim Biotelemetry (2016) 4:18 Page 10 of 12 Fig. 4 Photographic follow-ups with tagged whales. a Whale 20140601-6 tagged with two short (3 petals) titanium darts and again 2 and 34 days after tagging. b Whale 20140603-6 tagged with two long (6 petals) titanium darts and again 4 and 24 days after tagging. c Whale 20140604-5 tagged with two short (3 petals) and two long (6 petals) titanium darts and again 5 days after tagging and flexing movements, and usually feed in groups where and dove quickly. Mate et  al. [13] noted the reactions of whale-to-whale contact is common [32, 33]. Surface seven species of large whale to tagging, including reac- feeding can create additional drag forces from 2.5 to 5 tions as mild as head and fluke lifts, to evasive swimming times greater than animals at depth [34, 35]. Although we behavior, quick dives, and fluke swishes. In these other did not quantify prey during tagging, we observed tagged studies, the researchers noted that the responses to tag- humpback whales feeding on fish. These differences in ging were short-term, as was the case with this study. behavior due to foraging strategy could have influenced There have been few studies documenting healing fol - the duration that tags remained on humpback whales lowing tagging of large whales, especially with LIM- compared with duration on blue whales. PET and similarly designed darts. In developing early Response of animals to tagging with dart-attached tags implantable radio tags, Watkins et al. [12] found no signs did not elicit responses stronger than tagging with suc- of infection or tissue reaction at four tag-related wound tion cup-attached tags. Reactions ranged from no reac- sites 16–18  days post-attachment for humpback or fin tion to a hard tail flick. The range of reactions noted in whales. Mate et  al. [13] found that 40 re-sighted whales this study are consistent with the variability in reactions tagged between 1990 and 2005 exhibited varying levels of found within and among other species in a number of swelling or scarring at the tag site from implantable satel- previous studies [3, 36–39]. For example, Hooker et  al. lite tags; however, none were in poor health or showed [38] found no difference in observed response to tag signs of tissue sloughing at the tag site. Gendron et  al. deployments compared with biopsy sampling of north- [40] found extended periods of swelling when portions ern bottlenose whales (Hyperoodon ampullatus) and that of implantable tags remained embedded in tagged blue the behavioral state of the animal influenced the magni - whales. Best et  al. [41] reported scarring, but no swell- tude of the reaction. Watkins [39] noted that fin whales ing or difference in calving rates in re-sighted south - showed no reaction or moved away after being tagged; ern right whales (Eubalaena australis) that were tagged humpback whales had no reaction, swam faster, or fluked with implantable satellite tags. Similar to these studies, Szesciorka et al. Anim Biotelemetry (2016) 4:18 Page 11 of 12 Authors’ contributions follow-up photography of the site of tag attachment on AS, JC, and JH were involved in conception, study design, data collection and humpback whales up to 34  days after tagging indicated interpretation of the findings. AS collected and analyzed the data and was that the wounds exhibited no sign of tearing or swell- involved in laboratory analyses. AS, JC, and JH prepared the manuscript. All authors read and approved the final manuscript. ing, suggesting the modified darts had minimal physical impacts to the whales. Author details The four-dart configurations used in this study cre - Moss Landing Marine Laboratories, 8272 Moss Landing Rd, Moss Landing, CA 95039, USA. Cascadia Research Collective, 218 1/2 4th Ave W, Olympia, WA ated additional penetration points, each with the poten- 98501, USA. tial to allow for bacterial transfer inside the body [42]. However, the darts were small in width and length, Acknowledgements We thank Bill Watson and Kris Machado (MLML), for initial developments of tag thus limiting the depth of penetration into the blubber. attachment devices tested in this study. Thank you also to American Bench- Had the darts extended into the axial muscle, similar to mark Machine Works, especially Steve Jacobson and Jesse Brown, for creating implantable satellite tags, they would have been subject stainless steel barbs and plates for the tags. We also want to acknowledge Russ Andrews and Greg Schorr for ideas and discussions on dart design. Thank to the internal shearing forces between the blubber and you to the many volunteers that helped with tagging, especially James Fahl- muscle layers, creating deeper wounds in the blubber busch for his vital assistance in the field, Alison Stimpert for field assistance [40, 43]. and manuscript edits, Robin Baird for manuscript edits, and Nathan Harrison for assisting in some of the tag preparations. The tags also presented an opportunity to collect tis - sue samples. Although this is not a replacement for tradi- Competing interests tional biopsy methods, the collection of skin and blubber The authors declare that they have no competing interests. from suction cups and darts after the tags detached Availability of data and materials allowed us to lessen our physical contact with tagged The datasets analyzed during the current study are available from the cor- whales by not using traditional biopsy methods for this responding author on reasonable request. study. Tags retrieved up to 18 days after release from the Ethics approval and consent to participate animal yielded tissue samples that are being analyzed by All procedures performed were in accordance with the ethical standards Southwest Fisheries Science Center for the purpose of under MLML’s and Cascadia Research’s Institutional Animal Care and Use Committee protocols (#937 and #AUP-6, respectively), MLML’s and Cascadia sex identification. Research’s National Marine Fisheries Service Authorizations and Permits for Protected Species (#15271 and #16111, respectively), and MLML’s National Conclusions Oceanic and Atmospheric Administration Office of National Marine Sanctuar - ies multi-sanctuary research permit (#MULTI-2013-006). This study tested various tag attachment configurations to increase deployment duration of archival tags on large Funding whales while minimizing potential physical impacts to This research was funded by the Office of Naval Research [Grant No. N00014- 13-1-0772 to JC and Grant No. N00014-09-1-0632 to JH]. Additional funding whales. Tags with four-dart configurations with petals came from the American Cetacean Society, San Francisco Chapter; American resulted in the longest attachment durations on hump- Cetacean Society, Monterey Bay Chapter; California State University Council back and blue whales. The switch to heat-treated stain - on Ocean Affairs, Science and Technology; Dr. Earl Myers and Ethel M. Myers Oceanographic and Marine Biology Trust; California Professional Employer less steel allowed for the same tag attachment durations Organization; San Jose State University; David and Lucile Packard Foundation; as titanium, but with reduced dart or petal breakage. and Moss Landing Marine Laboratories [to AS]. Follow-ups with three tagged humpback whales indi- Received: 13 April 2016 Accepted: 1 September 2016 cated that the dart-attached tags created small wounds that showed no sign of tearing or swelling up to 34 days after tags detached. The use of dart-attached archival tags has presented new opportunities to collect high- resolution data over intermediate (weeks) time periods. References Although archival tags need to be recovered, these tags 1. Scholander P. Experimental investigations on the respiratory function in diving mammals and birds. Hvalradets Skrifter. 1940;22:1–131. can include a suite of high-sampling kinematic, acous- 2. Kooyman GL. Genesis and evolution of bio-logging devices: 1963–2002. tic, and environmental sensors. Using intermediate-term Mem Natl Inst Polar Res Ser. 2004;58:15–22. dart-attached archival tags, we can answer questions 3. Johnson M. Aguilar de Soto N, Madsen PT. Studying the behaviour and sensory ecology of marine mammals using acoustic recording tags: a about foraging efficiency, daily diving and transit activity, review. Mar Ecol Prog Ser. 2009;395:55–77. and diel trends. 4. Hazen EL, Maxwell SM, Bailey H, Bograd SJ, Hamann M, Gaspar P, Godley BJ, Shillinger GL. Ontogeny in marine tagging and tracking science: technologies and data gaps. Mar Ecol Prog Ser. 2012;457:221–40. Abbreviations 5. Goldbogen JA, Friedlaender AS, Calambokidis J, McKenna MF, Simon ARGOS: Advanced Research and Global Observation Satellite; C: celsius; GPS: M, Nowacek DP. Integrative approaches to the study of baleen whale global positioning system; LIMPET: low impact minimally percutaneous diving behavior, feeding performance, and foraging ecology. Bioscience. external-electronics transmitter; MLML: Moss Landing Marine Laboratories; 2013;63:90–100. SPOT: SPOT-257A satellite tag; TDR: time-depth recorder; VHF: very high 6. Norris KS, Evans WE, Ray GC. New tagging and tracking methods for the frequency. study of marine mammal biology and migration. In: Shevill WE, editor. Szesciorka et al. Anim Biotelemetry (2016) 4:18 Page 12 of 12 The whale problem: a status report. Cambridge: Harvard University Press; 27. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a 1974. practical and powerful approach to multiple testing. J R Stat Soc B. 7. Frost KJ, Lowry LF, Nelson RR. Radiotagging studies of belukha 1995;57:289–300. whales (Delphinapterus leucas) in Bristol Bay. Alaska Mar Mamm Sci. 28. Andrews RD, Baird RW, Schorr GS, Mittal R, Howle LE, Hanson MB. 1985;1:191–202. Improving attachments of remotely-deployed dorsal fin-mounted tags: 8. Scott MD, Wells RS, Irvine AB, Mate BR. Tagging and marking studies on tissue structure, hydrodynamics, in situ performance, and tagged-animal small cetaceans. In: Leatherwood S, Reeves RR, editors. The bottlenose follow-up. Seattle: Office of Naval Research; 2015. ONR Report Award dolphin. San Diego: Academic Press; 1990. Number: N000141010686. 9. Jeffries SJ, Brown RF, Harvey JT. Techniques for capturing, handling and 29. Shorter KA, Murray MM, Johnson M, Moore M, Howle LE. Drag of suc- marking harbour seals. Aquat Mamm. 1993;19:21–5. tion cup tags on swimming animals: modeling and measurement. Mar 10. Burgess WC, Tyack PL, Le Boeuf BJ, Costa DP. A programmable acoustic Mamm Sci. 2014;30:726–46. recording tag and first results from free-ranging northern elephant seals. 30. Croll DA, Tershy BR, Hewitt RP, Demer DA, Fiedler PC, Smith SE, Armstrong Deep-Sea Res Part II. 1998;45(7):1327–51. W, Popp JM, Kiekhefer T, Lopez VR, Urban J, Gendron D. An integrated 11. Fossette S, Ferraroli S, Tanaka H, Ropert-Coudert Y, Arai N, Sato K, Naito Y, approach to the foraging ecology of marine birds and mammals. Deep- Le Maho Y, Georges JY. Dispersal and dive patterns in gravid leatherback Sea Res Pt II. 1998;45:1353–71. turtles during the nesting season in French Guiana. Mar Ecol Prog Ser. 31. Wiley D, Ware C, Bocconcelli A, Cholewiak D, Friedlaender AS, Thompson 2007;338:233–47. M, Weinrich M. Underwater components of humpback whale bubble-net 12. Watkins WA, Schevill WE. The development and testing of a radio whale feeding behaviour. Behaviour. 2011;148(5–6):575–602. tag. Woods Hole: Woods Hole Oceanographic Institution; 1977. 32. Ware C, Friedlaender AS, Nowacek DP. Shallow and deep lunge feeding of 13. Mate B, Mesecar R, Lagerquist B. The evolution of satellite-monitored humpback whales in fjords of the West Antarctic Peninsula. Mar Mamm radio tags for large whales: one laboratory’s experience. Deep-Sea Res Sci. 2011;27(3):587–605. Part II. 2007;54(3–4):224–47. 33. Simon M, Johnson M, Madsen PT. Keeping momentum with a mouthful 14. Mate BR, Krutzikowsky GK, Winson MH. Satellite-monitored movements of water: behavior and kinematics of humpback whale lunge feeding. J of radio-tagged bowhead whales in the Beaufort and Chukchi seas Exp Biol. 2012;215:3786–98. during the late-summer feeding season and fall migration. Can J Zool. 34. Blake RW. Biological implications of the hydrodynamics of swimming at 2000;78:1168–81. or near the surface and in shallow water. Bioinspir Biomim. 2009;4:1–9. 15. Lagerquist BA, Mate BR, Ortega-Ortiz JG, Winsor M, Urban-Ramirez 35. Goldman JA. Eec ff ts of the free water surface on animals that jump out of J. Migratory movements and surfacing rates of humpback whales the water. Ph.D. thesis, Duke University, Durham, NC; 2001. (Megaptera novaeangliae) satellite tagged at Socorro Island, Mexico. Mar 36. Schneider K, Baird RW, Dawson S, Visser I, Childerhouse S. Reactions of Mamm Sci. 2008;24:815–30. bottlenose dolphins to tagging attempts using a remotely-deployed 16. Hooker SK, Baird RW. Diving and ranging behaviour of odontocetes: a suction-cup tag. Mar Mamm Sci. 1998;14:316–24. methodological review and critique. Mamm Rev. 2001;31(1):81–105. 37. Stimpert AK, Matilla D, Nosal E, Whitlow WLA. Tagging young humpback 17. Schorr GS, Falcone EA, Moretti DJ, Andrews RD. First long-term behavioral whale calves: methodology and diving behavior. Endanger Spec Res. records from Cuvier’s Beaked Whales (Ziphius cavirostris) reveal record- 2012;19:11–7. breaking dives. PLoS One. 2014. doi:10.1371/journal.pone.0092633. 38. Hooker SK, Baird RW, Al-Omari S, Gowans S, Whitehead H. Behavioral 18. Goodyear J. A new radio tag; the Remora, and behavior of a humpback reactions of northern bottlenose whales (Hyperoodon ampullatus) to whale (Megaptera novaeangliae). J Cetacean Res. 1981;2:1–2. biopsy darting and tag attachment procedures Fish. Bull. 2001;99:303–8. 19. Baird RW. Studying diving behavior of whales and dolphins using suc- 39. Watkins WA. Reaction of three species of whales Balaenoptera physalus, tion-cup attached tags. Whalewatcher: J Am Cetac Soc. 1998;31(1):3–7. Megaptera novaeangliae, and Balaenoptera edeni to implanted radio tags. 20. Andrews RD, Pitman RL, Ballance LT. Satellite tracking reveals distinct Deep-Sea Res. 1981;28(6):589–99. movement patterns for Type B and Type C killer whales in the southern 40. Gendron D, Martinez Serrano I, Ugalde de la Cruz A, Calambokidis J, Ross Sea, Antarctica. Polar Biol. 2008;31:1461–8. Mate B. Long-term individual sighting history database: an effective 21. Andrews RD. Improving attachments of remotely-deployed dorsal fin- tool to monitor satellite tag effects on cetaceans. Endang Species Res. mounted tags: tissue structure, hydrodynamics, in situ performance, and 2015;26:235–41. tagged-animal follow-up. Seattle: Office of Naval Research; 2011. ONR 41. Best PB, Mate B, Lagerquist B. Tag retention, wound healing, and subse- Report Award Number: N000141010686. quent reproductive history of southern right whales following satellite- 22. Clapham PJ. Humpback Whales. Stillwater: Voyageur Press; 1996. tagging. Mar Mamm Sci. 2015;31:520–39. 23. Katona S, Baxter SB, Brazier O, Kraus S, Perkins J, Whitehead H. Identifica- 42. Weller DW. Report of the large whale tagging workshop. San Diego: U.S. tion of humpback whales by fluke photographs. In: Winn HW, Olla BL, edi- Marine Mammal Commission; 2008. tors. Behavior of marine animals. Volume 3. Cetaceans. New York: Plenum 43. Moore M, Andrews R, Austin T, Bailey J, Costidis A, George C, Jackson K, Press; 1979. Pitchford T, Landry S, Ligon A, McLellan W, Morin D, Smith J, Rotstein D, 24. Sears R. The photographic identification of individual blue whales Balae - Rowles T, Slay C, Walsh M. Rope trauma, sedation, disentanglement, and noptera musculus in the Sea of Cortez. Cetus. 1987;7(1):14–7. monitoring-tag associated lesions in a terminally entangled North Atlan- 25. R Core Team. R: A language and environment for statistical computing. tic right whale (Eubalaena glacialis). Mar Mamm Sci. 2013;29:E98–113. R Foundation for Statistical Computing, Vienna, Austria. 2016; https:// www.R-project.org/. 26. Maxime Hervé. RVAideMemoire: Diverse Basic Statistical and Graphical Functions. R package version 0.9-55. 2016; https://CRAN.R-project.org/ package=RVAideMemoire.

Journal

Animal BiotelemetrySpringer Journals

Published: Sep 22, 2016

References