Land based observations occurred at Point Lena (58.39140 N, 134.77495 W) and Point Retreat (58.41308 N, 134.95644 W) (Figure 1). Data were collected using a Sokkia DT-5A theodolite connected to a laptop computer using the data acquisition software, Mysticetus¹. Data collection required a team of at least 3 people, consisting of a theodolite operator, computer operator, and 1–2 spotters. Humpback whales were observed using a Konus 20 × 60 spotting scope and Leica 10 × 42 binoculars. Behavioral events and states were classified using an ethogram (Table 2). During each field day, environmental variables, including visibility, cloud cover, precipitation, and Beaufort sea state, were collected every hour or as conditions changed. Due to daily tidal fluctuations of up to 5 m, theodolite station height was measured approximately every 15 min using vertical markers on the shoreline. To ensure reliable data collection, observations were made only in Beaufort sea state of ≤3, little or no rain, and <15 kt wind.

Humpback whale movement and behavioral data with respect to whale-watching vessel presence were collected using theodolite tracking methods described in Würsig et al. (1991) and behavioral observation methods described in Di Clemente et al. (2018). A “sighting” (i.e., observation period of behaviors for a humpback whale) began when an individual was spotted < 5 km from the field site. Focal follow observations with all-occurrence sampling (Altmann, 1974) was used to record behavioral events (Table 2) and continuous sampling was used to record behavioral state, heading, and number of vessels present within a 500 m radius of the whale at the time of the behavioral event. A 500 m threshold was used previously by Di Clemente et al. (2018) as an intermediate distance between distance thresholds previously used in whale-watching studies on humpback whales [300 m (Corkeron, 1995; Morete et al., 2007) and 1000 m (Gulesserian et al., 2011; Schaffar et al., 2013)]. Vessels were considered present when within 500 m of the whale and observed approaching, departing, or tracking (i.e., following a whale in a straight line or in a parallel line according to the last heading observed of the whale). Simultaneously, the theodolite was used to obtain successive latitude/longitude coordinates of humpback whale positions, which were plotted as polyline tracks on Mysticetus. A “track” of the individual included all positions recorded along with time, distance from field site, and number of vessels within 500 m. Distinct physical markings (e.g., unique coloration, scarring, fluke notching, or dorsal fin shape) were recorded throughout the observation to aid in confirming the focal animal. If a second humpback whale was spotted < 5 km from the theodolite station, sighting and track information were collected on both individuals as long as accuracy was maintained. Groups > 1 whale (e.g., bubble net feeding groups and mother-calf pairs) were not included in the dataset because the focal animal could not be reliably determined throughout the follow. However, this excluded only a small portion of the dataset.

No limit was set for the duration of sightings or tracks. The mean dive time for humpback whales in Southeast Alaska is <10 min (Dolphin, 1987), therefore a sighting ceased once an individual went undetected for >20 min or had been absent from the study area >10 min. An individual was considered “absent” if it was out of range (i.e., >5 km from the theodolite, verified on Mysticetus) or out of sight due to trees or presence of islands. This distance has been recommended for stations between 20 and 45 m above mean low sea level to reduce errors in precision from targets at greater distances (Würsig et al., 1991; Piwetz et al., 2018). This method was similarly used by Di Clemente et al. (2018) to minimize the chance of sampling an individual that was different from the original focal animal.

In the summer of 2017, 20 companies advertised whale-watching tours or charters in Juneau, AK (Schuler, unpublished data). The industry included vessels ranging in size from 8 to 32 m and accommodating between 6 and 144 passengers. Each vessel departed from Auke Bay Harbor (Figure 1), conducting up to 3 tours per day that averaged 2.5–3 h each. In addition to these commercial whale-watching vessels, private vessels would also opportunistically track humpback whales.

Summary statistics for deviation, speed, and IBI were calculated in the presence and absence of vessels (Table 4). The mean number of vessels observed for each fix was 0.8 ± 1.41 (range = 0 – 8). In the presence of vessels, 59.9% of fixes included more than one vessel (n = 743). The estimated whale deviation from their straight-line course was 38.9% higher in the presence of vessels than in the absence of vessels based on the AICc-best model (p < 0.001, Table 5). Using the number of vessels instead of vessel presence in the same model resulted in an estimated increase in deviation by 6.2% per additional vessel (p = 0.022), but the model had less support (ΔAICc = 14.77). Whale swimming speed was 5.4% faster in the presence vs. absence of vessels (p = 0.047, Table 6). However, the number of vessels did not have a significant effect on speed. While IBI was 6.7% shorter in the presence vs. absence of vessels (p = 0.025), AICc model comparisons indicated that a linear effect of the number of vessels on IBI resulted in a better model (ΔAICc = 5.78), suggesting a 3.4% decrease in IBI for each additional vessel (p = 0.001, Table 7). The categorical model for number of vessels did not indicate an obvious threshold effect for deviation, speed or IBI.

The mean percent time humpback whales were observed in the presence of vessels was 33% ± 39.2% (range = 1–100%) during tracks and 29% ± 36.7% (range = 1–100%) during sightings. During 40% of tracks and 44% of sightings, no vessels were present. During 16% of tracks and 11% of sightings, vessels were present for the entire time. Humpback whale directionality averaged 0.72 ± 0.308 (range = 0.01–1.00, n = 177) and RESP averaged 0.55 ± 0.26) breaths/min (range = 0.16–1.52, n = 201). Percent time spent in the presence of vessels did not significantly affect directionality. However, the best fit model for RESP included percent time spent with boats, behavioral state, date, and location, and indicated that the more time a whale spent in the presence of vessels during a track, the higher the RESP (p = 0.011).

A total of 5,489 behavioral events were recorded during 201 sightings (presence: 40.3%, n = 2213; absence: 59.7%, n = 3,276; Table 8). In the presence and absence of vessels, the predominant behavioral state observed was TRA (presence: 66.6%, absence: 76.1%), followed by FED (presence: 31.7%, absence: 21.5%), RES (presence: 1.4%, absence: 1.6%), and SAB (presence: 0.3%, absence: 0.8%). Markov chain analysis including TRA, FED, and SAB indicated that the transition probability between behavioral states differed by vessel presence (goodness-of-fit test, χ² = 33.4; df = 4; p < 0.001). In the presence and absence of vessels, whales were likely to continue engaging in FED and TRA (FED → FED, presence = 96.7%, absence = 95.7%; TRA → TRA, presence = 98.2%, absence = 98.5%). In the presence of vessels, SAB more frequently transitioned to FED (SAB → FED, presence = 42.9%, absence = 3.7%) or TRA (SAB → TRA, presence = 14.3%, absence = 7.4%), while in the absence of vessels, whales were more likely to continue SAB (SAB → SAB, absence = 88.9%, presence = 42.9%).

Monte Carlo simulations indicated that in the presence of vessels, the activity budgets of whales included less TRA and SAB (Figure 2). In the presence of whale-watching vessels, TRA composed 71.1% of the activity budget, compared to 80.7% in the absence of vessels, and SAB was 0.2% in the presence of vessels, compared to 0.9% in the absence of vessels. FED was also a large proportion of the activity budgets of whales, consisting of 28.6% in the presence of vessels and 18.4% in the absence (Table 9).

Horizontal movement metrics, such as changes in direction and increased swimming speed, are often used to identify vessel avoidance strategies by whales (Baker and Herman, 1989; Schaffar et al., 2013; Christiansen et al., 2014). The present study detected both a 38.5% higher deviation and 5% higher speed in the presence of vessels. Humpback whales have previously demonstrated increased path sinuosity (Schaffar et al., 2009; Stamation et al., 2010) and avoidance orientation in relation to vessels (Baker and Herman, 1989). Increased speeds in the presence of vessels has also been detected on humpback whale breeding grounds in the South Pacific (Schaffar et al., 2013) and South Atlantic (Morete et al., 2007). Direction changes and increased speeds are an energetically efficient strategy for humpback whales to avoid a perceived threat (Ford and Reeves, 2008; Senigaglia et al., 2016). While this ‘flight’ response may require less energy than a ‘fight’ response (i.e., surface-active behaviors) (Pitman et al., 2017), increased energetic expenditure spent avoiding vessels in highly trafficked areas, like Juneau, could be cumulative and decrease physical fitness over time.

Indicators of disturbance include changes in dive patterns and surfacing intervals (Bejder and Samuels, 2003). In the present study, shorter IBI in the presence of vessels indicates an increase in blow frequency. Furthermore, as the number of vessels increased, humpback whales exhibited significantly shorter IBI. These results support a meta-analysis by Senigaglia et al. (2016), which determined that mysticetes (i.e., baleen whales) tended to decrease IBI when whale-watching vessels were present. Previous studies in Juneau have also associated the presence of vessels with changes in breathing intervals (Baker et al., 1986) and increased variability in time spent at the surface (Peterson, 2001). Similarly, fin whales (Balaenoptera physalus) off the coast of Maine exhibited higher respiration rates and reduced dive durations, surface durations, and number of blows per surfacing sequence when whale-watching vessels were nearby (Stone et al., 1992). A decrease in IBI during interactions with whale-watching vessels can be of particular concern when it indicates a relative decrease in foraging efficiency, as seen in minke (B. acutorostrata) and fin whales (Christiansen et al., 2013b; Lesage et al., 2017). Furthermore, shorter IBI in the presence of vessels can reflect increased energetic expenditure and result in higher levels of oxygen consumption needed to recover (e.g., from increased speed to avoid vessels) (Christiansen et al., 2014).

As the percent time spent with vessels increased, the respiration rate increased. Over the course of a track, whales may be disturbed by vessel noise of tracking whale-watching vessels (Richardson et al., 1995) due to the strong or rapid changes in engine and propeller speed (Watkins, 1986). Alterations in whale breathing patterns to persistent vessel exposure can indicate vessel avoidance of these sound levels. Multiple vessels simultaneously tracking a whale will accentuate this effect (Holt et al., 2009). Vessel characteristics (e.g., size and engine type) and vessel approach (e.g., angle and speed) are also likely to elicit different responses in whales. However, these factors could not be isolated due to the large proportion of humpback whale observations collected in the presence of >1 vessel. Furthermore, while the present study considered vessels present as those tracking whales within 500 m, it is likely that the vessel detection range for whales is >500 m (Baker and Herman, 1989; Richardson et al., 1995) as cetaceans respond to stimuli as far as tens of kilometers away (Baker and Herman, 1989; Richardson et al., 1995). Therefore, disturbance from vessel noise may be heightened in heavily trafficked areas, like Juneau. While not measured in the current study, information regarding detectable ranges of vessel engine sound in the tour area, and observations of whale movement and behavior with larger vessel distance thresholds, would help to validate this supposition.

The present study reflects results from data collected in Juneau by Di Clemente et al. (2018), which demonstrated that humpback whale activity budgets in the presence of vessels consisted of less traveling and more feeding than in the absence of vessels. This could also reflect that whale-watching tours are more likely to select a feeding whale to watch over a traveling whale. However, humpback whales did not alter their feeding or traveling behaviors based on vessel presence. Previous research in Alaska has indicated that feeding humpback whales are less likely to alter their behavioral state in response to approaching vessels than non-feeding whales (Krieger and Wing, 1984, 1986; Peterson, 2001), suggesting that the need to build energy reserves while on the feeding grounds supersedes abandoning feeding even if disturbed. Responses may also occur beneath the surface, such as decreases in humpback whales feeding efficiency as seen with increased sound levels from vessels (Blair et al., 2016). By contrast, minke whales in Faxafloìi Bay, Iceland, decreased feeding behavior as a result of whale-watching vessel presence (Christiansen et al., 2013b). Differences in observed responses may vary by prey type, prey densities, and availability of food elsewhere (Krieger and Wing, 1986). Furthermore, the low number of recorded transitions between traveling and feeding could reflect the inability of shore-based observations to confirm humpback whales feeding at depth. Due to the importance of feeding in the area, it is possible that some straight, directional movement observed at the surface, could have also included feeding beneath the surface.

The only significant effect of vessel presence on humpback whale activity budgets was with respect to surface active behavior. Similar to Di Clemente et al. (2018), humpback whales in the absence of vessels were more than twice as likely to continue surface active behaviors, and whales in the presence of vessels were twice as likely to transition from surface active behavior to traveling. In other studies in Alaska, humpback whales increased surface active behaviors in the presence of vessels, potentially representing aggressive (e.g., tail breaching and lob tailing) and negative responses to vessels (Baker and Herman, 1989; Peterson, 2001). Transitions from vocal communication to non-vocal surface-generated communication (i.e., breaching, tail-slapping) by humpback whales have also been detected in noisy environments (i.e., increased background noise, high wind speeds) (Dunlop et al., 2010). However, surface active behavior has also been attributed to communication to distant groups (Kavanagh et al., 2017). This indicates that cessation of surface active behavior could result from acoustic masking due to vessel noise and subsequent inability to communicate (Richardson et al., 1995; Gabriele et al., 2018). However, due to the relatively small proportion of time whales spend resting and in surface active behaviors, in comparison to feeding and traveling, a larger sample size is needed to support the findings of the present study.

The present study did not directly address long-term consequences of vessel presence; however, it is possible that the measured short-term effects on whale movement and behavior could have cumulative effects on individuals and local populations in areas of high disturbance. Increased energetic expenditure and potential decreases in feeding efficiency, as evidenced by increased direction changes, higher traveling speeds, and changes in breathing and diving patterns, could have negative long-term effects. Prolonged energetic expenditure due to vessel avoidance behaviors may deplete energy reserves and disrupt homeostasis, ultimately causing physical fitness decline in whales (Beale, 2007). These physiological consequences, if extreme enough, could cause population decline, influencing reproductive success or decreasing chances of survival (Bejder and Samuels, 2003).

Humpback whales exhibit a high degree of feeding site fidelity (Calambokidis et al., 2001; Weinrich and Corbelli, 2009) to both general feeding areas (Baker et al., 1990) and to specific regions within the feeding grounds (Weinrich, 1998; Stevick et al., 2006). This may be an adaptive strategy to maximize prey intake by feeding on “known” prey resources that are predictable in time and space (Stevick et al., 2006). Humpback whales that remain in highly trafficked areas despite high exposure to vessel presence and associated stressors may do so because they rely on the resources from that area or they no longer perceive the presence of vessels as a threat.

Negative effects on whales may be minimized over time by habituation to vessel presence (Watkins, 1986). On the New England feeding grounds, Watkins (1986) determined that since whale watching began in 1976, humpback whales in the presence of vessels are more likely to continue their previous activity or respond by approaching vessels. Furthermore, despite high vessel pressure in the Juneau tour area, several individual humpback whales continue to return in subsequent years, often being observed multiple times a season (Teerlink, 2017). In a study by Teerlink et al. (2018), humpback whales in the Juneau area at the end of a whale-watching season (September) did not exhibit higher levels of the stress hormone, cortisol, compared to more remote regions. The lack of physiological stress responses detected in humpback whales in Juneau could indicate that repeated short-term disturbances may not be causing chronic stress. However, it is also possible that whales more sensitive to the presence of vessels had already left the tour area to avoid vessels, and the samples of whales in Juneau were biased toward whales more tolerant of vessels (Bejder et al., 2006a).

The expansion and persistence of vessel presence could result in alteration of humpback whale ranging patterns or habitat utilization. Changes in humpback whale distribution in an effort to avoid vessels could be detrimental not only to the whales, but to the profitability of the Juneau tour industry. In nearby Glacier Bay, habitat abandonment by humpback whales in response to vessel exposure has already been documented (Dean et al., 1985). Similarly, individual humpback whale singers in Brazil have responded to high vessel traffic by either moving out of recording range or discontinuing songs (Sousa-Lima and Clark, 2008). Bottlenose dolphins in Milford Sound, New Zealand have also adjusted their seasonal residency patterns in response to heavy vessel traffic (Lusseau, 2005).

Regulations were established in Alaska to prevent “take,” defined under the MMPA as an action to “harass, hunt, capture, or kill, or attempt to harass, hunt, capture, or kill any marine mammal.” The present study revealed that there are significant differences in short-term whale movement and behavioral patterns in the presence of vessels. This indicates that the current regulations, including to “not disrupt the normal behavior or prior activity of a whale” (Table 1), may not be adequate to reduce takes of humpback whales. Therefore, revisiting the humpback whale approach regulation and expanding the existing vessel approach limit to create a larger buffer around the whales should be considered by management to help reduce vessel impacts on humpback whales. The present study also determined that changes in deviation and IBI occurred in response to the number of vessels. Restrictions on the maximum number of vessels around whales or limits to the number of vessels in the industry does not currently exist. Managing the number of vessels watching whales would minimize vessel effects on whale movements and behavior.

The management approach in Alaska should continue to be supplemented with education programs encouraging operator participation in voluntary best practices. Whale SENSE was introduced in Alaska in 2015 (NOAA Fisheries Whale and Dolphin Conservation, 2018). In 2018, 44% of the companies that offered dedicated whale-watching tours in Juneau participated in the program, consisting of approximately 67% of vessels in the industry (Schuler, unpublished data). This program aims to minimize harassment of whales through the education of naturalists, captains, and passengers and promotion of responsible whale-watching practices. Programs such as Whale SENSE can help to manage tourist viewing expectations and encourage operator compliance (Filby et al., 2015). By combining evidenced-based regulations with effective educational programs, a sustainable whale-watching industry can be maintained.