Beluga, Delphinapterus Leucas, Ethogram: a Tool for Cook Inlet Beluga Conservation?

Beluga, Delphinapterus leucas, Ethogram: A Tool for Cook Inlet Beluga Conservation?

MARIAN HOWE, MANUEL CASTELLOTE, CHRISTOPHER GARNER, PAUL MCKEE, ROBERT J. SMALL, and RODERICK HOBBS

Introduction and accurately (Müller et al., 1998), ing displayed by orca, Orcinus orca as well as understood in terms of their (Martinez and Klinghammer, 1978), An ethogram is a catalogue of mu- causative and functional bases (Pur- are specific to only that species. Even tually exclusive and objective behav- ton, 1978). The establishment of a ba- though an ethogram based on the be- iors or actions exhibited by an animal sic ethogram is essential to the pursuit haviors of one population is widely that avoids subjectivity and functional of further behavioral analyses of any accepted as not representative for the inference as to their possible purpose. given species (Scheer et al., 2004). species as a whole, that ethogram can It is a key tool that helps to quantify Despite the potential value of an serve as a reference and standard to species-specific behaviors by describ- ethogram to behavioral studies, only understand basic species traits and to ing the discrete, basic motor patterns a few are available for a select num- inform species management decisions. that form the behavioral repertoire of ber of species (Scheer et al., 2004). Utilizing an ethogram to study a a given species (Kikkawa and Thorne, For marine mammals, the behavior of species of concern will provide a 1971; Martin and Bateson, 2007). By which has been studied extensively, valuable tool to the emerging field of describing and defining the behavioral the lack of ethograms cataloging their “conservation behavior,” which uses inventory of a species as an ethogram, behaviors is surprising (a complete list the proximate and ultimate aspects of behaviors among different populations of studies that include cetacean etho- animal behavior to aid conservation may be compared more thoroughly grams is given in Appendix A). The decisions and reduce the loss of biodi- majority of cetacean ethograms focus versity (Buchholz, 2007). The conser- on Tursiops (e.g., Mann and Smuts, vation of cetacean species may benefit Marian Howe was with the Alaska Department 1999; von Streit et al., 2011), includ- from ethogram use, as cetaceans are of Fish and Game, 333 Raspberry Road, An- ing perhaps the most comprehensive known to exhibit behavioral changes chorage, AK 99518, and is currently with the Hawaii Institute of Marine Biology, 46-007 Lili- marine mammal ethogram, developed in response to a wide variety of anthro- puna Road, Kaneohe, HI 96744. Manuel Castel- by Müller et al. (1998), who built upon pogenic disturbances including navy lote and Roderick Hobbs are with the National Marine Mammal Laboratory, Alaska Fisheries previous observations to describe over sonar, aircraft overflight, ship traffic, Science Center, National Marine Fisheries Ser- one hundred behaviors of the bottle- ice breaking, and marine construction vice, NOAA, 7600 Sand Point Way N.E., Se- nose dolphins, Tursiops truncates, ob- (Richardson et al., 1995; Southall et attle, WA 98115-6349. Christopher Garner is with the Department of Defense, Joint-Base served along the San Diego coastline. al., 2007). In addition, the response Elmendorf Richardson, Anchorage, AK 99506. Some of the behaviors described of bowhead whales, Balaena mysti- Paul McKee is with the U.S. Fish and Wildlife in the cetacean ethograms, such as cetus, and possibly other cetaceans to Service, 1011 East Tudor Road, Anchorage, AK 99503. Robert J. Small is with the Alaska leaping, are shared among differ- these anthropogenic disturbances var- Department of Fish and Game, 1255 West 8th ent species (Norris and Dohl, 1979; ies with behavioral activity (Beale and Street, AK 99811-5526. Dudzinski, 1996; Müller et al., 1998), Monaghan, 2004; Ellison et al., 2012). doi: dx.doi.org/10.7755/MFR.77.1.3 while other behaviors, such as spray- A complete catalog of behaviors for

ABSTRACT— We present the first peer-re- ity of observing specific beluga behaviors with anecdotal observations of whale ac- viewed wild beluga, Delphinapterus leucas, in Eagle Bay and Eagle River (Knik Arm, tivity in the bay, and we encourage further whale ethogram, a comprehensive descrip- Cook Inlet). Behaviors were observed and investigation to more fully explain our re- tion and definition of behavioral states and recorded from 2007 to 2011 between May sults. The explicit language used to define events exhibited by the endangered stock and December when belugas are known this beluga ethogram will facilitate a more of Cook Inlet beluga whales (CIBWs). The to forage in the study area. We found that standard approach to behavioral studies of ethogram can be used to help quantify be- CIBWs are generally more likely to travel CIBWs, provide a means to quantify the re- luga behaviors and increase the utility of fu- than mill in Eagle Bay, except when the tide sponse of CIBWs to anthropogenic activi- ture and ongoing beluga behavioral studies, is ebbing and above its midpoint, and that ties, and allow comparison among multiple in Cook Inlet and for other populations. We traveling occurred more frequently in Eagle populations. Thus, this CIBW ethogram will tested the applicability of the ethogram by River than in either the north or south sec- potentially promote innovative approach- quantitatively examining spatial, temporal, tions of the bay. The results of our quantita- es to help manage the endangered CIBW and environmental effects on the probabil- tive behavioral analysis can be compared population.

32 Marine Fisheries Review a cetacean may thus help researchers ton, 2000; Hobbs et al., 2005; Rugh et activities associated with the remedia- quantify changes in observed behavior al., 2010). It is our hope that this belu- tion of white phosphorus residues. due to different levels and types of dis- ga whale ethogram will serve as a ref- turbance for a cetacean population in- erence for future behavioral studies of Ethogram habiting an anthropogenically-altered CIBWs and other beluga populations. We developed our ethogram oppor- environment and assist in directing We also describe how CIBW behaviors tunistically from a U.S. Army moni- management efforts. vary by tide state and location within toring project of CIBWs in Eagle One endangered stock that may ben- Eagle Bay, demonstrating how the ap- Bay and Eagle River. Observations of efit from a behavior-based manage- plication of our ethogram can increase CIBWs were carried out from 2007 ment approach is the Cook Inlet stock both ecological and behavioral knowl- to 2011 between the months of May of beluga whales (Delphinapterus leu- edge of CIBWs over varying temporal and December when belugas gather cas). This small population has been and spatial scales. Such knowledge in Eagle Bay (Huntington, 2000) and geographically isolated from other be- will help direct future studies of CIB- feed in Eagle River. Observations were luga populations for over 10,000 years Ws concerning their response to hu- conducted by two or three experienced and is also the most genetically dis- man disturbances within their critical observers using 12x45 power binocu- tinct of the species (O’Corry–Crowe habitat. lars and high-powered spotting scopes et al., 1997; Laidre et al., 2000). The from the north shore at the mouth of size of the Cook Inlet beluga whale Methods Eagle River, an advantageous sur- (CIBW) population decreased by half Study Area vey location to view whales through- between 1994 and 1998, primarily due out Eagle Bay and in the mouth of the to unsustainable subsistence harvests, Cook Inlet is a tidal estuary locat- river. ed in south-central Alaska and covers and has continued to decrease by 1.6% 2 During the 2007 field season, belu- annually since 1999 (Hobbs et al., an area of approximately 20,000 km ga observation protocol followed the 2000; Hobbs et al., 2015). with 1,350 km of coastline (Rugh et ad libitum sampling technique (Alt- The geographic range of CIBWs al., 2005). Extreme tidal fluctuations mann, 1974), with general field notes has also contracted substantially over with a 9 m range result in strong cur- recorded when belugas entered Eagle the last several decades, with very few rents up to 9–10 knots and tidal bores, Bay. From these observations, multiple whales observed in lower Cook Inlet which constantly alter the shoreline beluga behaviors were initially defined during the summer months and the (Moore et al., 2000). Our CIBW be- and described. Beginning in 2008, a area of highest concentration in the havioral studies were conducted in more systematic sampling approach upper inlet near Anchorage, the largest Eagle Bay and Eagle River, which are was employed, which consisted of a city and port in Alaska (Rugh et al., located in Knik Arm, upper Cook Inlet group follow protocol and focal group 2010). The CIBW was federally listed (Fig. 1). sampling method (Altmann, 1974). as an endangered species in 2008, pri- Glacially-fed Eagle River flows Observers tracked a group of whales marily because of the lack of popula- through Eagle River Flats, a 866 ha over the course of a 20-min sampling tion recovery after regulation of the estuarine marsh on Joint-Base Elmen- period and defined the activity of the Alaska Native subsistence hunt, a rela- dorf-Richardson, before emptying into group based on the behavioral state of tively small geographic distribution, Eagle Bay. A complex interaction of the majority of whales during the pe- and concerns about long-term popu- physical forces influences the marine riod. A “group” of whales was defined lation viability (Hill and DeMaster, system of Cook Inlet, including those as the number of estimated animals 1998; NMFS1). Because very little re- exerted by a high tidal range, glacial- sufficiently close in proximity to po- search was conducted on CIBWs prior fluvial effects from multiple river in- tentially be confused with each other to their endangered listing, a dearth of puts, high degree of sedimentation, (Mann and Smutts, 1999). A behavior and the subarctic coastal climate of literature exists on their basic ecology 2 that occurred over an extended period and behavior, and factors currently im- southcentral Alaska (Lawson et al. ). of time, such as milling, was consid- peding recovery are unknown. Direct anthropogenic influences on ered a “state” (Martin and Bateson, In this paper we present an ethogram the study area are largely centered on 2007). of CIBW behaviors observed from the flats and include military training, Within each sampling period, we es- May to December 2007 to 2011 in Ea- both historic (Army artillery impact timated the number of whales using gle Bay and Eagle River in Knik Arm area since 1949) and current (winter instantaneous scans over the 20-min in the upper Cook Inlet, a frequent fall firing of artillery into flats), as well as period, though estimates were usually gathering area for the whales (Hunting- made within the first 10 min of the 2Lawson, D. E., L. E. Hunter, S. R. Bigl, B. M. Nadeau, P. B. Weyrick and J. H. Bodette. 1996. round after counting all of the indi- 1NMFS (National Marine Fisheries Service) Physical system dynamics, white phosphorus viduals in a group(s), trying to mini- 2008. Conservation plan for the Cook Inlet be- fate and transport, 1994, Eagle River Flats, Fort luga whale (Delphinapterus leucas). NMFS, Of- Richardson, Alaska. CRREL Rep. 4 p. prep. for mize double counting. Whales were fice of Prot. Res., Juneau, AK, 122 p. U.S. Army Alaska, Fort Richardson. also classified as white, gray, or calf,

77(1) 33 and the location of whale groups at the start of each sampling round was ap- proximated, based on a 8 x 6 cell grid superimposed on a map of Eagle Bay and Eagle River (Fig. 1). Each cell represented a 1 km2 area. At the end of each day, an estimate of the total number of whales was made by add- ing up the total number of individuals counted across all independent whale observations per the study protocol. During the 2011 field season, the beluga observation protocol was expanded for whales that entered Ea- gle River. Specifically, we included a fine-scale behavioral component, or “event,” which we defined as a discrete behavior, such as flapping, that occurs at a certain point in time (Martin and Bateson, 2007). When an individual whale performed an event in the river, observers recorded the type of event, the time, and the state of the majority of the whales in the river at that time. Events were only recorded for whales in Eagle River up to the first turn in the river (Fig. 1) because of their proximity to observers, while states continued to be recorded for whales in both Eagle River and Eagle Bay. Systematic observations were made on the Cook Inlet whales between 2008 and 2011. As our knowledge of the beluga behavioral repertoire has expanded, we constructed an ethogram of beluga behaviors frequently viewed in Eagle Bay and Eagle River and have added to it as new behaviors are described. Between 2008 and 2011 Figure 1.— Location of Eagle River and Eagle Bay in Knik Arm, Cook Inlet, Alas- we also continued to refine and edit ka, and superimposed grid for recording beluga whale visual locations. 1 cell=1 descriptions of the behaviors to be in- km2 area. CIBWs only found in cells 1, 2, 3, 4, 7, 8, 9, 10, 13, 14, 15, 16, 19, 20, cluded in the ethogram. We present the 21, 22, 25, 26, 27, 28, 31, 32, 33, and 39. Observations of whales in Eagle River ethogram in two categories, states and conducted in mark “A” location and up river to mark “B”. Map projection in WGS events, with video and photographs 84, UTM Zone 6 North (meters), declination 19° E. compiled for each behavior.

Testing the Applicability havior of belugas in Eagle Bay and Ea- tshawytscha, runs, rivers with medi- of the Ethogram gle River and analyze the frequency of um flow accumulation, tidal flats, and This ethogram was developed to behaviors to corroborate the apparent areas with sandy coastlines (Moore et provide standard definitions so that relationship between tidal fluctuations al., 2000; Goetz et al., 2007; Goetz beluga behaviors could be quantified and beluga movements and behaviors et al., 2012). Daily beluga movement and to standardize future studies in- in the study site. patterns, however, are largely deter- volving Cook Inlet beluga life history On a large temporal scale, belu- mined by tides, and in upper Cook In- and ecology, thus enhancing our over- ga distribution within Cook Inlet is let, it is believed that beluga travel is all understanding of their biology. We based primarily on proximity to rivers associated with tidal currents and di- used the ethogram to describe the be- with Chinook salmon, Oncorhynchus rection (Ezer et al., 2008). Specifical-

34 Marine Fisheries Review ly, with a flooding tide belugas move adjacent to the previously referenced individually and then combined into up Knik Arm to utilize typically inac- sandbar. For each 20-min period, tidal similar tide categories. We then used cessible mudflats and river mouth ar- information from the Port of Anchor- Akaike Information Criterion (AIC) in eas for foraging (Ezer et al., 2008). age tide station maintained by the R in a stepwise elimination to identify In Eagle Bay, during the ice-free National Oceanic and Atmospheric the most parsimonious model. months the belugas seem to move and Administration was corrected with a behave in a fairly predictable pattern half hour delay to account for the dis- Results relative to the tide cycle, though these tance between the Port of Anchorage Ethogram conclusions have been based solely and Eagle Bay. on anecdotal evidence collected from The tide cycle was divided into six The ethogram described here fol- 2007 to 2011 in conjunction with the categories: flood tide upper half and lows the standard structure suggested beluga monitoring project around Ea- lower half, ebb tide upper half and by Martin and Bateson (2007) includ- gle River Flats. lower half, at high tide or at low tide. ing events and states. Video sequenc- After about a half of the ebb cycle, Belugas were not observed in the bay es of all the definitions below can be belugas travel south from areas north during high tides, so we combined the found at https://www.youtube.com/ of the bay with the outgoing tide. remaining tide cycles into five catego- watch?v=4x7N0NoHgnU. Images of Some bypass Eagle River, but usually ries: EbbAbove, EbbBelow, Flood- feeding behavior provided by Stacy at least one group enters the river and Above, FloodBelow, and Low. DeRuiter. mills or travels up and down the river Finally, behavior differences were until about three-quarter ebb. Those thought to occur between August States that entirely bypass the river seem to and the later months based on anec- 1) Milling: Whales surfacing in a move west and mill along the shore un- dotal observations made from Eagle more or less constantly varying direc- til they reach the sandbar at the south- River Flats so two time periods, “Au- tion, especially in relation to each oth- ern end of the bay, where they remain gust” and “months other than August,” er. They may remain in the same area to mill or leave the bay. When the tide were considered. Only data from 2011 or drift/move with the tide or current. begins to flood, the whales actively were used, as observations from only 2) Traveling: Whale or whales moving travel, following the flooding current 2011 provided sufficient information in a consistent, unidirectional fashion across the mudflats to the north end of to determine tide states for each 20- relative to other individuals in a group. Eagle Bay. By three-quarters flood, the min observation period. Each 20-min Traveling whales typically appear to whales have disappeared around the observation period from 2011 with move in a purposeful, coordinated north point of the bay on their way to whales present and either milling or manner, most often with the direc- upper arm areas that are probably only traveling in these grid areas was in- tion of the tidal current. An exception accessible at or near high tide. cluded in the analysis. Periods without to this rule is that when traveling in Wheras these anecdotal patterns beluga sightings were omitted. rivers, whales may travel against the seem to be typical of the belugas in With the probability of the logged water flow. A single traveling whale Eagle Bay in the ice-free months, their behavior as the dependent variable, moves forward with few to no lateral actual probability and frequency had and location, tide categories, and deviations in course. not yet been documented. The etho- month as the independent variables, gram provides a method to classify we used logistic regression (glm) in Events these behaviors by time period so that the statistical computing language and 1) Bubbling: A whale blows under- the probability of seeing a behavior environment R version 2.13.1 (http:// water or near the surface and creates a can be related to the environmental cran.r-project.org/) and the code edi- cloud of bubbles that splash at the sur- variables, thus allowing quantification tor Tinn-R version 1.16.1.4 (http:// face. This definition does not include of beluga movement patterns. www.sciviews.org/Tinn-R/)) to esti- the normal exhalation that sometimes For this analysis, we consider the mate the probability of observing trav- occurs immediately prior to surfacing. two most frequently observed behav- eling as a behavior for a given 20-min 2) Fast Dive: Similar to the div- ioral states, milling and traveling, as interval in each area, under different ing behavior state but more rapid and they were easily assessed across the tide categories and during August vs always accompanied by significant entire study area compared to individ- later months. We consider an additive surface disturbance from the beat- ual behavioral events, which generally model: ing tail fluke. The acute downward require close proximity to the whale. angle bending may be absent or less Eagle Bay was separated into three ar- Probability(traveling behavior) ~ dramatic. eas (Fig. 1): “North Bay” (grid areas tidequarter, #+ Bay.Location + 3) Feeding: Whale usually observed 4, 10, 16, 22, 28, 34), the “River” (ar- Augustday, in the “prey pursuit” (no. 7 below) be- eas 33, 39, 40), and “South Bay” (ar- havioral event just prior to feeding. eas 31, 32, 25, 26), which is located with all categories initially represented The distinction between the two events

77(1) 35 is that a prey item is observed in the or during this event to avoid confusion 14) Unknown: Behavior not fully whale’s mouth during feeding but not with social interactions. observed; observer cannot confidently during prey pursuit. Visual observation 8) Side-scanning: Whale swims (of- place behavior into one of the estab- of prey in a whale’s mouth is extreme- ten very slowly) at the surface with the lished event categories. ly rare, owing to the turbid waters of lateral aspect of its body visible. The Knik Arm combined with the tenden- pectoral flipper, lateral surface of the Testing the Applicability cy for belugas to ingest prey whole. body, tail fluke, or a combination of of the Ethogram To capture instances when prey was these parts, is visible, often for 30 sec to A total of 659 h 40 min of obser- not observed in a whale’s mouth, yet several minutes. This behavioral event vations from 3 June until 14 Dec. feeding had likely occurred, we added is often followed by explosive move- 2011 were collected. From these, 64 the following language to the defini- ments of the tail as the animal moves h 20 min were made in the presence tion of a feeding event: a prey-pursuit rapidly forward in pursuit of prey. of belugas and were included in the event which includes a whale driving 9) Snorkeling: A surfacing whale analysis. a prey item onto land or into the air, lifts its head gently to the surface in In the initial analysis we found that followed by observation of a whale or such a manner that only the melon, EbbBelow (estimate = 1.53 (SE = pursuit wake at the point of prey re- blowhole, and a small portion of the 0.56), z = 2.76, p < 0.01), FloodAbove entry into the water, and the observer dorsal surface just posterior to the (estimate = 2.36 (SE = 0.83), z = 2.83, has more than 50% confidence that the blowhole are visible. After gas ex- p < 0.01), FloodBelow (estimate = 1.90 prey item was captured (e.g., as indi- change has occurred, the whale then (SE = 0.60), z = 3.18, p < 0.01), and cated by a violent surface disturbance gently lowers its head below the sur- Low tide (estimate = 1.92 (SE = 0.78), at the point of reentry followed by an face. The dorsal ridge is never seen z = 2.45, p < 0.01) categories were sta- immediate cessation of observable ac- during a snorkeling event. Note that tistically different from EbbAbove, but tivity); note that all three conditions this behavior often makes detection not from each other, and so they were must be met for this secondary defini- of whales difficult from a distance as grouped together for further analysis tion to apply. it reveals only a small portion of the so that the tide quarter variable was 4) Flapping: Pectoral or caudal fin whale and leaves a rapidly dissipated, either EbbAbove or not. The stepwise slams the surface and creates splash. relatively small (several feet diam- process removed the Augustday vari- Multiple flapping in sequence is con- eter), concavity at the surface of the able, as date was not found to have any sidered a single event, unless another water. effect on the probabilities, leaving the event is observed between flapping. 10) Social Interaction: Typically probability to be determined by the lo- 5) Floating: Whale observed at the two, but sometimes more, whales en- cation and whether or not the tide was surface with some portion of its body gage in physical contact, chasing each in the EbbAbove category. visible for an extended period of time other, or tail flapping each other, al- The final logistic regression model (typically 10 sec or more) and with ways followed by one of the individu- was used to calculate the probabilities little to no directed movements. The als moving away from the other. This of observing travelling behavior when whale moves passively with the cur- event does not apply to mother-calf the tide was ebbing and was above half rent and does not transition into prey interactions. for that cycle (EbbAbove) for each bay pursuit as often seen in side-scanning 11) Spy Hopping: Whale emerges location. Across all locations, traveling (no. 8 below). from the water with its head held ver- is more frequently observed during the 6) Normal Dive: Surfacing whale tically above the water, to at least eye grouped tide quarters than during the bends its dorsal surface at an acute level, but without the pectoral flippers EbbAbove tide quarter (Fig. 2A). Dur- downward angle, slipping beneath the being above the water’s surface, and ing the grouped tide quarter, traveling surface of the water with the tail flukes remains in this position for at least is significantly more likely to occur in usually emerging completely out of several seconds before submerging Eagle River than either north or south the water and being the last part of vertically with its head submerging Eagle Bay, while milling is significant- the whale seen prior to complete sub- last. The eyes are usually observed in ly more likely to occur in the north sec- mergence; this action is slow, almost a spy-hopping beluga. tion of the bay than in the river. During casual. 12) Tail up: Caudal fin and some- the EbbAbove tide quarter, belugas 7) Prey Pursuit: Whale exhibits sud- times part of the peduncle is observed are in general more likely to be mill- den or explosive movements, often above the surface, as if the whale is ing (Fig. 2B), but when traveling, the forward but may include rapid changes diving, but these remain in the air for belugas are more likely to be found in in direction and depth, always result- an extended period of time (5 sec or the river than any other area of the bay. ing in a fast-appearing linear wake, more). violent disturbance of water, or a com- 13) Other: Behavior exhibited by Discussion bination of the two. No interactions whale does not fall into one of the es- In total we cataloged two behavioral between whales are observed prior to tablished event categories. states and thirteen behavioral events

36 Marine Fisheries Review the tidal analysis contradicted the ex- pected movement and behavioral patterns of the whales in Eagle Bay. For example, the data analysis shows that CIBWs more frequently mill than travel in the bay only when the tide is ebbing and above its midpoint. As the whales will move as far up the arm as possible during the high tide (Ezer et al., 2008), it may be that the majority of CIBWs traveled up Knik Arm and out of sight with the incoming tide and had not yet returned to the bay during that tide quarter. There was a small group of whales during the study period that was noted to swim against the tide at times and to enter Eagle Bay when the majority of whales were not present. It is possible that the behavior of these outliers influenced this result. The other major finding of the analysis was that CIBWs more frequently travel in Eagle River during all tide stages than in any other area of Eagle Bay. In general, we observed more milling in the north and south areas of the bay as compared to the river. In contrast, anecdotal observations have suggested that the whales travel down from the north in Eagle Bay during the Figure 2.—The probabilities of observing belugas in the behavioral state of travel- ebbing tide with some whales stop- ing (A) and milling (B) at above half tide level during an ebb tide versus all other ping to mill in Eagle River. The higher tide stages combined, in three different areas of Eagle Bay and Eagle River, Knik probability of observing milling in the Arm, Alaska, 2011. north and south regions may be due to the fact that milling inherently occurs over a greater temporal scale whereas displayed by the Cook Inlet beluga CIBW behavioral patterns were found traveling through an area occurs more whales in Eagle Bay and Eagle Riv- to significantly vary with these vari- quickly; thus as the analysis was a er to establish the first peer-reviewed ables within the study area. Other ce- function of duration of beluga obser- ethogram for wild beluga whales. In taceans, such as the bowhead whale, vation, the chances of observing mill- contrast with the extensively described also exhibit behaviors that correlate ing in a given area were greater than behaviors for Tursiops (Müller et al., with naturally varying factors includ- those of traveling. 1998) and Stenella longirostris (Norris ing season and water depth (Würsig It is less clear why CIBWs appear to and Dohl, 1979), the range of behav- et al., 1984; Richardson et al., 1995). travel more in the river than any other iors shown by CIBWs is quite small, We found a relatively high probability area. One possible explanation is that which is explained, in part, by the lack of observing whales traveling during the current of Eagle River forces the of aerials in the beluga behavioral rep- the majority of the tide cycle, which whales to continually travel with or ertoire and by the turbid water present in general supports previous anecdotal against the direction of the river cur- in Cook Inlet, which prevents identifi- observations. This result makes logical rent. The current at the mouth of the cation of behavior occurring below the sense, as average current velocity in river is slower and may be more con- immediate surface layer. Cook Inlet is around 3 kn but can ex- ducive to milling, and thus the whales We also demonstrated one applica- tend up to 12 kn (Moore et al., 2000); would likely expend less energy mill- tion of the ethogram, the quantification thus the whales will expend less ener- ing just outside Eagle River than with- of behavioral patterns exhibited by gy traveling with the current than mill- in the river itself. Another possible CIBWs, in relation to location within ing potentially against the current. explanation that may operate in con- Eagle Bay and tide stage and level. However, some of the results of junction with the previous reasoning

77(1) 37 is that the primary foraging grounds in whales may exhibit behaviors further standardizing the behavioral language Eagle River for CIBWs may be upriver out in Eagle Bay that would not be of CIBWs. and out of sight of observers on Eagle entirely visible to observers stationed In addition, we show with our etho- River Flats. Hence, the whales would at the mouth of Eagle River. gram a correlation between CIBW frequently be observed traveling in the Furthermore, CIBWs may exhibit behavioral state and environmental river in order to access their foraging different behaviors in other areas of variables. Future studies should focus sites. Further investigation using the Cook Inlet, as unusual events have on whether CIBW behavioral states ethogram of the specific events ex- been recorded for whales observed are influenced by anthropogenic dis- hibited by CIBWs in Eagle River will in the Little Susitna River (Easly- turbances such as seismic operations provide a more complete explanation Appleyard et al.4). Because of these in Cook Inlet. Studies on bowhead of these behavioral patterns. limitations, our ethogram may under- whales demonstrate that traveling We also acknowledge that certain represent the total number of behav- whales spend less time near the sur- sources of error may have affected iors displayed by CIBWs and thus the face when in the vicinity of seismic our tidal analysis. Some of the unex- catalog may be expanded to include operations, while feeding and socializ- pected behavioral results, such as fre- new behaviors observed in the future; ing whales were more tolerant of such quent milling in the north bay, may however, we believe that the present activities (Robertson et al., 2013). Re- stem from unknown, uncontrollable ethogram provides a general illustra- cent seismic activities in Cook Inlet variables in Knik Arm, such as varia- tion of behaviors one might observe in have included requirements to suspend tions in local bathymetry or the size this population. operations when protected marine and timing of upper Cook Inlet salm- mammals, like CIBWs, are observed on runs. Observer bias may have also Conservation Implications entering a defined activity zone.6 How- played a role, as six different observ- The goal of this study was to de- ever, if CIBWs’ sensitivity to this dis- ers documented CIBW states, and velop an ethogram for CIBWs and turbance increases under a certain there may have been discrepancies demonstrate its quantitative use to behavioral state, like travelling for between their categorizations of states enhance understanding of CIBW be- instance, observers may miss CIBWs and events. havioral patterns. Facilitating coopera- during their surveys (e.g., Miller et al. Furthermore, it is widely admit- tion among scientists studying CIBW 2005; Harwood et al. 2010), as might ted that individual differences in the behaviors is of particular importance happen if the whales spent more time behavior of wildlife should be con- due to the whales’ endangered status. underwater. Thus, with continued sidered when analyzing a population. Moreover, the integration of visually development in Cook Inlet, under- Individual differences in age, sex, observed behaviors with acoustic be- standing and quantifying how human size, aggressiveness, learning ability, havior can further expand knowledge activities alter CIBW response in the past experience, heterozygosity, and a of CIBW life history and ecology. context of a given behavioral state will myriad of other variables can all affect Several recent and ongoing CIBW result in more accurate density and how an animal reacts to a given situa- monitoring projects in Cook Inlet, in- population estimates near these opera- tion and may determine the success or cluding a remote photo-based moni- tions (Robertson et al., 2013). failure of a management strategy or a toring study (Easly-Appleyard et al.4) In Eagle River and Eagle Bay spe- conservation initiative (Festa-Bianchet and a photo-identification project (Mc- cifically, military activities may in- and Apollonio, 2003). Guire et al.5) incorporate a behavioral fluence CIBW behavior, yet without In addition, the use of both the fo- component. We hope that our etho- objective and definitive descriptions cal group sampling method and the gram will enable greater collabora- of behavioral states and events, there fine-scale behavioral sampling has tion among these various groups and has been no way to quantify the level several limitations in the develop- encourage more behavioral studies by of behavioral changes caused by these ment of our ethogram. First, behav- activities. Our study demonstrates the ioral sampling in the study area is frequency of CIBW behavioral pat- limited to activities above the water 4Easly-Appleyard, B., L. Pinney, L. Polasek, J. terns relative to naturally occurring line due to the extreme turbidity of PEasley-Appleyard, B., L. Pinney, L. Polasek, J. factors, which provides a CIBW be- Knik Arm. In the future, greater in- Prewitt, and T. McGuire. 2011. Alaska SeaLife havior baseline in the absence of direct Center Cook Inlet beluga whale remote monitor- tegration of DIDSON sonar imaging ing Pilot Study. Final Rep. from Alaska SeaL- human disturbances. Further standard- (Sound Metrics Corp.3) into the mon- ife Center, Seward, 49 p. (http://www.fakr.noaa. ized behavioral observations of CIBW itoring project may provide a better gov/protectedresources/whales/beluga/survey/ in Eagle Bay and Eagle River concur- cib_susitna093011.pdf). understanding of subsurface CIBW rently with military operations will al- 5McGuire, T., and C. Kaplan. 2009. Photo-iden- behaviors. It is also possible that the tification of beluga whales in upper Cook Inlet, Alaska. Final rep. of field activities in 2008. 6Editorial, 2012. Responsible seismic operations 3Mention of trade names or commercial firms Rep. prep. by LGL Alaska Res. Assoc., Inc., An- in Cook Inlet, Alaska. Accessed 22 Aug. 2013. does not imply endorsement by the National chorage, for Nati. Fish and Wildl. Found., Chev- http://www.apachecorp.com/News/Articles/ Marine Fisheries Service, NOAA. ron, and ConocoPhillips Alaska, Inc. View_Article.aspx?Article.ItemID=2480

38 Marine Fisheries Review low for a comparison of the observed cal and behavioral activities. Ph.D. Dissertat., marine mammals – southeastern Beaufor Sea, CIBW behavior with and without hu- Texas A&M Univ. Coll. Stat., 215 p. 2001–2002. In S. L. Armsworthy, P. J. Cran- Ellison, W. T, B. L. Southall, C. W. Clark, and ford, and K. Lee (Editors), Offshore Oil and man disturbances, and thus enabling A. S. Frankel. 2012. A new context-based ap- gas environmental effects monitoring: ap- researchers to quantify the responses proach to assess marine mammal behavioral proaches and technologies, p. 511–542. Bat- responses to anthropogenic sounds. Conserv. of CIBWs to these operations. telle Press, Columbus, Ohio. Biol. 26:21−28. Moore, S. E., K. E. W. Shelden, L. K. Litzky, B. Finally, with the likely development Ezer, T., R. Hobbs, and L. Oey. 2008. On the movement of beluga whales in Cook Inlet, A. Mahoney, and D. J. Rugh. 2000. Beluga, of a hydroelectric dam in the Little Alaska. Oceanography 21(4):186–195. Delphinapterus leucas, habitat associations in Susitna River in the next few years, Festa-Bianchet, M., and M. Apollonio. 2003. Cook Inlet. Mar. Fish. Rev. 62(3):60–80. and its potential impacts on CIBW Animal behavior and animal conservation. Is- Müller, M., H. Boutière, A. Weaver, and N. land Press, Wash. D.C., 394 p. Candelon. 1998. Ethogram of the bottlenose anadromous prey (Alaska Energy Au- Goetz, K. T., D. J. Rugh, and R. C. Hobbs. 2007. dolphin (Tursiops truncates) with special ref- thority7), the ability to unambiguous- Habitat use in a marine ecosystem: beluga erence to solitary and sociable dolphins. Vie ly define CIBW foraging behaviors whales Delphinapterus leucas in Cook Inlet, Milieu 48(2):89–104 [Engl. transl.]. Alaska. Mar. Ecol. Prog. Ser. 300:247–256. Norris, K. S., and T. P. Dohl. 1979. Behavior of around construction events, may pro- ______, R. A. Montgomery, J. M. Ver the Hawaiian spinner dolphin, Stenella longi- vide insight into changes in the behav- Hoef, R. C. Hobbs, and D. S. Johnson. 2012. rostris. Fish. Bull. 77(4):821–849. Identifying essential summer habitat of the ior of belugas in response to changes O’Corry-Crowe, G. M., R. S. Suydam, A. endangered beluga whale Delphinapterus Rosenberg, K. J. Frost, and A. E. Dizon. in prey distribution and availability, or leucas in Cook Inlet, Alaska. Endang. Spec. 1997. Phylogeography, population structure Res. 16:135–147. Doi: 10.3354/esr00394 and dispersal patterns of the beluga whale changes in the Susitna Delta itself re- Harwood, L., T. Smith, A. Joynt, D. Kennedy, R. sulting from changes in hydrology or Pitt, S. Moore, and P. Millman. 2010. Poten- Delphinapterus leucas in the western Ne- siltation. tial for displacement of whales and seals by arctic revealed by mitochondrial DNA. Mol. seismic and exploratory drilling activity in Ecol. 6:955–970. 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77(1) 39 Appendix: development in wild bottlenose dol- Salden, D. R. 1979. Supplementary observations phin newborns (Tursiops sp.). Behaviour concerning an ethogram of the killer whale Cetacean Ethograms by Species 136(5):529–566. (Orcinus orca L.). Carnivore 2(3):17–18. Müller, M., H. Boutière, A. Weaver, and N. Atlantic spotted dolphin Candelon. 1998. Ethogram of the bottlenose Short-finned pilot whale (Stenella frontalis) dolphin (Tursiops truncates) with special reference to solitary and sociable dolphins. Vie (Globicephala macrorhynchus) Dudzinski, K. M. 1996. Communication and Milieu. 48(2):89–104, [Engl. trans.]. Hofmann, B., M. Scheer, and I. P. Behr. 2004. behavior in the Atlantic spotted dolphins von Streit, C., G. Udo, and L. von Fersen. 2011. Underwater behaviors of short-finned pilot (Stenella frontalis): relationships between vo- Ethogram of two captive mother-calf dyads whales (Globicephala macrorhynchus) off cal and behavioral activities. Ph.D. Dissertat., of bottlenose dolphins (Tursiops truncates): Tenerife. Mammalia 68(2–3):221–224. Texas A&M Univ. Coll. Sta., p. 196–204. Comparison with field ethograms. Aquat. Scheer, M. 2010. Review of self-initiated be- Herzing, D. L. 1996. Vocalizations and associ- Mamm. 37(2):193–197. haviors of cetaceans directed towards human ated underwater behavior of free-ranging Weaver, A. C. 1987. An ethogram of naturally swimmers and waders during open water en- Atlantic spotted dolphins, Stenella frontalis occurring behavior of bottlenose dolphins counters. Interact. Stud. 11(3):442–466. and bottlenose dolphins, Tursiops truncatus. (Tursiops truncatus) in southern Californian ______, B. Hofmann, and I. P. Behr. 2004. Aquat. Mamm. 22:61–79. waters. Masters thesis, San Diego State Univ., Ethogram of selected behaviors initiated by Miles, J. A., and D. L. Herzing. 2003. Under- San Diego, Calif. 360 p. free-ranging short-finned pilot whales (Glo- water analysis of the behavioural develop- bicephala macrorhynchus) and directed to ment of free-ranging Atlantic spotted dolphin Tucuxi (Sotalia guianensis) human swimmers during open water encoun- (Stenella frontalis) calves (birth to 4 years of ters. Anthrozoös 17(3):244–258. age). Aquat. Mamm. 29(3):363–377. do Nascimento, L. F., P. I. A. P. Medeiros, and M. E. Yamamato. 2008. Description of the Spinner dolphin Bottlenose dolphin (Tursiops spp.) surface behavior of marine tucuxi, Sotalia guianensis, at Pipa Beach. Psicologia: Re- (Stenella longirostris) Chechina, O. N, and N. L. Kondratieva. 2009. flexao & Critica 21(3):509. Norris, K. S., and T. P. Dohl. 1979. Behavior of Formation of probabilistic structure of motor the Hawaiian spinner dolphin, Stenella longi- behavior in bottlenose dolphins in captivity. Orca (Orcinus orca) rostris. Fish. Bull. 77(4):821–849. Zhurnal Vysshei Nervnoi Deyatelnosti Imeni I P Pavlova 59(5):587–592. Martinez, D. R., and E. Klinghammer. 1978. A Mann, J., and B. Smuts. 1999. Behavioural partial ethogram of the killer whale. Carni- vore 1:13–27.

40 Marine Fisheries Review Errata Howe, M., M. Castellote, C. Garner, P. McKee, R. J. Small, and R. Hobbs. 2015. Be- luga, Delphinapterus leucas, ethogram: A tool for Cook Inlet beluga conservation? Marine Fisheries Review 77(1):32–40.

The paper inadvertently states in the fi rst sentence of the Abstract (p. 32) and the fi rst sentence of the Discussion section (p. 36–37), that it presents the fi rst peer-reviewed ethogram of wild belugas. The paper does present the fi rst peer-reviewed ethogram of Cook Inlet beluga whales; however, t he fi rst ethogram of wild belugas was developed by Smith et al., 1994, and that citation is added to the Appendix on page 40:

Beluga whale (Delphinapterus leucas)

Smith, T. G., M. O. Hammill, and A. R. Martin. 1994. Herd composition and behaviour of white whales (Delphinapterus leucas) in two Canadian arctic estuaries. Bio- science 39:175–184.

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