Humpback whales feed on hatchery-released juvenile salmon

Humpback whales are remarkable for the behavioural plasticity of their feeding tactics and the diversity of their diets. Within the last decade at hatchery release sites in Southeast Alaska, humpback whales have begun exploiting juvenile salmon, a previously undocumented prey. The anthropogenic source of these salmon and their important contribution to local fisheries makes the emergence of humpback whale predation a concern for the Southeast Alaska economy. Here, we describe the frequency of observing humpback whales, examine the role of temporal and spatial variables affecting the probability of sighting humpback whales and describe prey capture behaviours at five hatchery release sites. We coordinated twice-daily 15 min observations during the spring release seasons 2010–2015. Using logistic regression, we determined that the probability of occurrence of humpback whales increased after releases began and decreased after releases concluded. The probability of whale occurrence varied among release sites but did not increase significantly over the 6 year study period. Whales were reported to be feeding on juvenile chum, Chinook and coho salmon, with photographic and video records of whales feeding on coho salmon. The ability to adapt to new prey sources may be key to sustaining their population in a changing ocean.

EMC, 0000-0001-8451-7880 Humpback whales are remarkable for the behavioural plasticity of their feeding tactics and the diversity of their diets. Within the last decade at hatchery release sites in Southeast Alaska, humpback whales have begun exploiting juvenile salmon, a previously undocumented prey. The anthropogenic source of these salmon and their important contribution to local fisheries makes the emergence of humpback whale predation a concern for the Southeast Alaska economy. Here, we describe the frequency of observing humpback whales, examine the role of temporal and spatial variables affecting the probability of sighting humpback whales and describe prey capture behaviours at five hatchery release sites. We coordinated twicedaily 15 min observations during the spring release seasons 2010-2015. Using logistic regression, we determined that the probability of occurrence of humpback whales increased after releases began and decreased after releases concluded. The probability of whale occurrence varied among release sites but did not increase significantly over the 6 year study period. Whales were reported to be feeding on juvenile chum, Chinook and coho salmon, with photographic and video records of whales feeding on coho salmon. The ability to adapt to new prey sources may be key to sustaining their population in a changing ocean.

Background
Humpback whales (Megaptera novaeangliae) are notable among baleen whales for their diet diversity. Their large flukes and long pectoral fins allow for quick acceleration and manoeuvring, enabling humpback whales to capture highly mobile prey [1]. This energetically demanding filter feeding requires prey to be aggregated for capture by humpback whales [2,3]. Humpback whales demonstrate particularly complex and sometimes innovative foraging tactics [4][5][6][7]. Behavioural plasticity may be an important aspect of their persistence by allowing them to adapt to changing environments and avoid competition [8,9].
Humpback whales feed primarily on euphausiids and small schooling fish [10][11][12]. In Southeast Alaska, the humpback whale population has been increasing since the end of commercial whaling in the early 1970s [13][14][15]. Increased intraspecific competition can lead to an increase in a population's diet diversity with the inclusion of less-preferred prey items [9]. Humpback whales have not been documented feeding on wild juvenile salmon (Salmonidae) in the scientific literature despite the fact that juvenile salmon numerically dominate the inshore and coastal waters of Southeast Alaska [16] and some species of juvenile salmon have been found in schools or aggregations [17]. A review of the scientific literature revealed a single reference for salmon as prey for humpback whales [18]. Klumov [18] found adult pink salmon (Oncorhynchus gorbuscha) in the stomachs of humpback whales feeding near a run in the Kuril Islands of Russia.
Despite the lack of scientific record, hatchery personnel observed humpback whales feeding on juvenile salmon along shore near a release site as early as 1999. In 2008, a humpback whale was video recorded at Hidden Falls hatchery (electronic supplementary material, S1). In recent years (2011,2015,2016) of historically poor returns of chum salmon, hatchery managers have implicated humpback whale predation. Modified rearing and release protocols have been implemented to minimize humpback whale predation [19][20][21], but the success of these strategies is difficult to measure.
The objectives of this study were to document juvenile salmon as prey for humpback whales in Southeast Alaska, model the main factors affecting the probability of sighting humpback whales at release sites and describe humpback whale foraging behaviours at these sites.

Study area
This study was located at five hatchery release sites in protected coves on the eastern side of Baranof Island in Southeast Alaska, adjacent to Chatham Strait, a deep (up to 600 m), 240 km long, 15 km wide channel within the Alexander Archipelago (figure 1). Three different organizations participated in data collection at five release sites: Hidden Falls, managed by the Northern Southeast Regional Aquaculture Association (NSRAA); Takatz (NSRAA); Mist Cove (NSRAA); Little Port Walter (NOAA) and Port Armstrong (Armstrong Keta Inc. collection. Behavioural observations were conducted at each of the five release sites over 6 years (2010-2015). Each site was systematically sampled twice a day, once in the morning and once in the afternoon. Observation times were selected by observers at the beginning of each season and remained consistent throughout the season to prevent biasing observations towards low-probability events. Whale observations outside of the predetermined sampling times were designated separately as opportunistic sightings. Observations were to begin about a week prior to releases and conclude one to two weeks after releases, when possible. Observations were recorded on standardized forms, with information on humpback whale presence, abundance and behaviours (sleeping/logging, breaching, surface feeding), as well as the presence of other possible salmon predators. Forms included a list of physical barriers whales may have used to aid in prey capture. This list was modified from a list of barriers compiled by the Glacier Bay Humpback Whale Monitoring Programme (C. Gabriele 2017, personal communication) to include net pens and docks in addition to surface, shoreline, tide-rip and kelp. Observers also noted the timing, location, species, abundance, age and mass of juvenile salmon released. During the coho salmon release at Hidden Falls in 2014, photography and videography were used to document feeding events (Go Pro Hero 4).
To determine which factors affected the presence of humpback whales at release sites, we modelled the probability of sighting a whale at a hatchery release site using a logistic generalized linear model (GLM) and Akaike Information Criteria (AICc)-based model selection [27,28]. Tested covariates included release site, year and a categorical variable for timing of the observation period relative to releases. Staff occasionally extended their observations beyond 15 min, which could increase the probability of sighting a whale. We, therefore, included observation duration as a covariate, and all model results were presented based on model predictions for a 15-min observation period:  For observations conducted after the final release, an additional covariate (f.release) for the number of elapsed days since the last release was included.
For k = after ln π j(k=after) where π j(k=after) is the probability of observing a whale in year i at site j after the final release at that site has occurred (i.e. k = after) where other variables are defined identically to the above and f.release is an ordinal variable that expresses the number of days that have elapsed since the final release at a particular site in a particular year.

Humpback whale feeding behaviour at release sites
Observers recorded data on the presence or absence of humpback whales during 2252 observation periods at five hatchery release sites over 6 years. Humpback whales were reported to be targeting releases of Chinook, chum and coho salmon. For each of these three species, whales were observed feeding when no other species had been released from that site. Underwater video and photographs showed humpback whales targeting coho salmon at Hidden Falls hatchery in 2014 (figure 2; electronic supplementary material, S2). When humpback whales were noted near the release sites (n = 124 sightings), 81% of those sightings were of single individuals (n = 100); 10% of whale observations had a group size of 2 (n = 13) and 9% were 3 or more whales (n = 11) with a single observation of 10 animals, although this group was specifically noted as feeding on herring (Clupea pallasii). For 60% of observations when whales were sighted (n = 75), at least one barrier was noted. For the remaining 40% of whale sightings (n = 49), observers did not note feeding in the presence of a feeding barrier, noted that no feeding barrier was present or were uncertain. The most common barriers noted other than the surface (presumed for any observed feeding events) were shoreline (42%), bubbles (27%), dock or net pen (16%), tide (5%) and kelp (2%). Multiple feeding barriers were recorded in 26% of observations. In addition to these feeding behaviours, whales were noted as sleeping/logging (i.e. holding stationary at the surface; 2%) and breaching (5%).

Probability of sighting a whale
When modelling the probability of whale sightings over all time periods, the best models included site, timing and observation duration as explanatory variables (table 1). The probability of whale sightings increased notably once salmon were released (figure 3). Probability of whale sightings was highest at the Takatz and Hidden Falls sites, and lowest at Port Armstrong. As expected, the probability of a whale sighting increased with observation duration. Overall, the probability of whale sightings decreased with year, but year was not included in the top-ranked model (including year resulted in AICc = 0.6 from the top model).      Table 2. Top candidate logistic models for describing the probability of sighting a humpback whale at a release site (response) after releases have concluded. All models include an intercept term. The full model (EQ2) is shown here as the second-ranked model. K is the total number of parameters, AICc is the Akaike Information Criterion adjusted for sample size. AICc is the difference between the AICc for each model and the AICc for the top-ranked model.

Discussion
Here we document humpback whales feeding on a novel prey. These feeding events were documented with direct observations as well as photographic and videographic evidence from the hatchery release sites. Using standardized observation methodology, we determined that humpback whale presence was closely associated with the release of juvenile salmon. Hatchery-released salmon were abundant in the region for only a few decades [23] before whales began to exploit them annually at multiple sites. The rapid release of large numbers of juvenile hatchery salmon, which differs from the protracted marine migration of their wild conspecifics, probably increased their profitability as prey for humpback whales, which rely on dense aggregations of prey. Wild Chinook and coho salmon in particular are known for agonistic behaviours and diffuse distributions [29,30], which may make them atypical prey for filterfeeding whales in a natural system. The extent to which humpback whales may target wild salmon or hatchery-released salmon after their outmigration from the release sites is unknown. As expected, humpback whales were most common while releases were in progress; however, whales were also seen prior to and following releases. It is possible that pre-release humpback whale observations reflect whales assessing the prey field periodically in anticipation of a release but only spending time there when sufficient prey are encountered. Prey anticipation by Dolly Varden (Salvelinus malma) has been noted at release sites in Southeast Alaska (E. Prestegard 2016, personal communication) and by sculpin (Cottus spp.) anticipating spawning sockeye salmon (O. nerka) [31]. The decline in whale sightings after releases have concluded is best explained by a decrease in prey availability due to the dispersal and mortality of juvenile salmon from the release area. These local declines in humpback whale sightings were notable because they occur despite a concomitant seasonal increase in humpback whale populations in the region [15].
Hidden Falls and Takatz had the highest rates of whale sightings. Hidden Falls and Port Armstrong release the greatest biomass of salmon each year, but Takatz and Hidden Falls are located near each other and are not truly independent, with whales and potentially also salmon moving between these areas. Hidden Falls, Takatz and Mist Cove also tend to release salmon later than more southerly sites. The later timing of these releases (May and June) compared to Port Armstrong (April and May) may correspond with more whales present on the feeding grounds following their spring migration [15].
While at release sites, humpback whales often fed near physical barriers. Whales feeding near barriers may simply be a result of salmon distribution near these structures, or conversely feeding near barriers could be a tactic used by whales for aggregating prey or impeding prey escape. The frequent use of bubbles offered stronger evidence of forced prey aggregation. Feeding near barriers has been observed and noted by Glacier Bay National Park researchers for decades (Glacier Bay 2017, unpublished data). It has also been offered as an explanation for the use of bubbles to corral prey as well as near shore, tidally mediated and surface-feeding behaviours [32][33][34]. These behaviours may be necessary to aggregate Chinook and coho salmon into a sufficient density for profitable feeding, as these species do not school as densely as pink, chum or sockeye salmon juveniles [17,35]. Species preference could not be directly tested because at Hidden Falls and Port Armstrong, multiple species were released in succession, with overlapping presence at the release site. In addition, species releases at single-species sites were confounded by differences in biomass, release timing and location.
Despite the increase in humpback whales regionally and the relatively recent introduction of hatchery salmon as a prey source, we found no evidence of an increasing trend in humpback whale predation at release sites across years. One explanation is that the resource is currently being fully exploited at these release sites and the prey or habitat characteristics cannot support more frequent feeding. It is also possible that hatcheries are not particularly favourable places to feed compared to other foraging opportunities available to humpback whales. This is supported by the observation of whales feeding predominantly as individuals rather than feeding aggregations. Finally, it may be too soon to detect an increase over the substantial interannual variability. Even if these sites are fully exploited, hatchery predation could still be spreading to other releases sites in the region. If recent increases in the humpback whale population both locally and throughout the North Pacific [13,14] result in increased intraspecific competition, one possible outcome is increased dietary diversity of the population via individual specialization on less-preferred prey [36].
The interaction between humpback whales and an anthropogenically derived food source bears further investigation as both a novel predator-prey interaction and for the potential economic impact. Future studies will directly test whether high humpback whale predation on a salmon cohort at the point of release is related to poor marine survival of released salmon and assess the economic impacts of that predation to local fisheries. During this study, hatchery staff noted many strategies for mitigating predation, primarily aimed at reducing the density of salmon aggregations at the releases site. One of the most widespread methods was to release fish slowly over time, a strategy known as a 'trickle' release as opposed to a more traditional 'mass' release. Staff also tried releasing fish at night, on an outgoing tide, or in a less sheltered location. The most intensive strategy employed by NSRAA was to release salmon at a larger size so that they will move from the littoral habitat more quickly [21]. A longitudinal study in space and time will be necessary to isolate the effects of these strategies on marine survival. Future studies will also characterize the prey field at release sites to determine the prey quality associated with foraging at hatchery release sites.
Phenotypic plasticity in foraging behaviour offers advantages over strict specialization under certain conditions [8]. Phenotypic plasticity that leads to dietary diversity across time, space or among individuals can be an important evolutionary strategy to persist or thrive in changing environmental conditions [7] or high intraspecific competition [9]. The resulting behavioural innovations may be a key reason why humpback whale populations have recovered so successfully in much of the world [37] and Southeast Alaska, in particular [14].