Relative importance of local enhancement as a search strategy for breeding seabirds: an experimental approach

Animal Behaviour 106 (2015) 71e78

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Relative importance of local enhancement as a search strategy for breeding seabirds: an experimental approach Kevin R. Bairos-Novak, Kevin A. Crook, Gail K. Davoren* Department of Biological Sciences, University of Manitoba, Winnipeg, MB, Canada

a r t i c l e i n f o Article history: Received 2 December 2014 Initial acceptance 5 February 2015 Final acceptance 27 March 2015 Published online xxx MS. number: A14-00976 Keywords: Atlantic puffin capelin common murre decoy foraging behaviour local enhancement memory northern gannet search strategy

During the breeding season, seabirds may use many behavioural strategies to reduce the time and energy spent searching for patchily distributed prey. Seabirds breeding at a large colony on the northeast Newfoundland coast (Funk Island), primarily common murres, Uria aalge, and northern gannets, Morus bassanus, predominantly feed on capelin, Mallotus villosus. Within foraging ranges, high-abundance capelin aggregations can be predictably located at deep-water (<40 m) spawning sites during the spawning period in mid- to late July, before which capelin are distributed in small, ephemeral schools. To investigate the 'local enhancement' hypothesis, we conducted a field-based experiment by deploying seabird-mimicking plastic models, or 'decoys', during JulyeAugust in 2009 and 2013, to determine whether breeding murres, gannets and Atlantic puffins, Fratercula arctica, respond to seabird aggregations. We used three decoy treatments: ‘Murre’, ‘Gannet’ and ‘Hotspot’ (both murre and gannet decoys). Pursuit-diving and plunge-diving birds were 4e7 and 17 times, respectively more likely to respond to decoy treatment relative to control periods. All species responded more to conspecifics, or to species within the same foraging guild, during single-species treatments (i.e. Murre, Gannet), but responded similarly (i.e. murres, puffins) or more (i.e. gannets) to the Hotspot treatment, suggesting that predator density in general is an important cue. Fewer murres responded to decoys during capelin spawning relative to pre-spawning, suggesting that murres use local enhancement to a lesser degree when prey can be predictably located nearby. This study provides experimental evidence that seabirds use local enhancement as a search strategy, but to varying degrees under changing prey conditions. © 2015 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Owing to the vastness of the ocean, energy costs of locating profitable prey patches by marine predators can be high. Therefore, the evolution of behavioural strategies to minimize energetic costs within the ecological context of a species' foraging environment should maximize fitness (Thiebault, Mullers, Pistorius, & MezaTorres et al., 2014). For animals living or foraging in groups, there is potential for trade-offs between relying on previous experience (e.g. memory) and using social information to locate profitable prey patches (Dall, Giraldeau, Olsson, McNamara, & Stephens, 2005). These trade-offs are likely driven by the reliability of social information available and the predictability of prey locations. Numerous studies have documented marine predators making foraging trips to a few distinct locations over the short term during breeding seasons (e.g. Garthe, Montevecchi, & Davoren, 2007; Garthe,

* Correspondence: G. K. Davoren, Department of Biological Sciences, 212B Biological Sciences Building, 50 Sifton Rd, University of Manitoba, Winnipeg, MB R3T 2N2, Canada. E-mail address: [email protected] (G. K. Davoren).

Montevecchi, & Davoren, 2011; Hamer, Phillips, Hill, Wanless, & Wood, 2001; Irons, 1998; Montevecchi, Benvenuti, Garthe, Davoren, & Fifield, 2009), nonbreeding seasons (e.g. Gende & Sigler, 2006; Sigler et al., 2012), as well as on an annual scale (e.g. Clapham et al., 1993). These forays to the same location over the short and long term suggest memory-based foraging on predictable prey aggregations, which ultimately may minimize energetically costly search activities (Gende & Sigler, 2006). Within areas of predictable high prey density, predators may further reduce energy expenditure by using area-restricted search patterns (Einoder, Page, Goldsworthy, De Little, & Bradshaw, 2011; Paiva, Geraldes, Ramirez, Garthe, & Ramos, 2010; Weimerskirch, Pinaud, Pawlowski, & Bost, 2007), to concentrate search effort where prey is most likely encountered (Einoder et al., 2011; Hamer et al., 2009), or has been encountered before (Weimerskirch et al., 2007). When prey cannot be predictably located, however, an alternative strategy may be local enhancement (i.e. predators cueing to the foraging activities of other predators; Dall et al., 2005). For local enhancement to be profitable, other predators feeding on similar prey must be easily detected (e.g. high densities, high visibility) and

http://dx.doi.org/10.1016/j.anbehav.2015.05.002 0003-3472/© 2015 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

K. R. Bairos-Novak et al. / Animal Behaviour 106 (2015) 71e78

reliably indicate the location of prey patches with high enough densities to minimize competitive interactions (Thiebault, Mullers, Pistorius, & Meza-Torres et al., 2014). There are a growing number of studies illustrating that seabirds cue to the foraging activities of conspecifics (e.g. Grunbaum & Veit, 2003; Thiebault, Mullers, Pistorius, & Meza-Torres et al., 2014, Thiebault, Mullers, Pistorius, & Tremblay, 2014; Tremblay, Thiebault, Mullers, & Pistorius, 2014) and allospecifics (e.g. Camphuysen & Webb, 1999; Davoren, Garthe, Montevecchi, & Benvenuti, 2010) to locate prey. The reliability of information obtained from a different species depends on whether the allospecific feeds on similar prey types and whether it enhances or reduces the availability of prey. Pursuit-diving birds are often classified as initiators (sensu Bayer, 1983), as they dive below the prey aggregation, driving prey to the surface (Camphuysen & Webb, 1999; Hoffman, Heinemann, & Wiens, 1981) and making prey available to aerial predators. The foraging activities of aerial predators often attract other species (catalysts, joiners; sensu Bayer, 1983; Hoffman et al., 1981), thereby forming mixed-species feeding assemblages. These assemblages may break up, however, when they are joined by species whose foraging activities reduce the accessibility of prey (suppressors; sensu Hoffman et al., 1981), such as pursuit-plunging birds that disperse prey in the water column. On the northeast Newfoundland coast, capelin, Mallotus villosus, are the focal forage fish species (Carscadden & Vilhjalmsson, 2002). The Funk Island Seabird Ecological Reserve lies approximately 60 km from the northeast Newfoundland coast (Fig. 1a), where high numbers of common murres, Uria aalge, and northern gannets, Morus bassanus, breed. Both species rely on capelin to adequately provision themselves and their chicks upon hatching in mid- to late July (Davoren, 2007; Davoren & Montevecchi, 2003; Montevecchi, 2007), although gannets also incorporate larger pelagic fish (e.g. herring, salmon) when available nearby (Montevecchi, 2007). In this region, capelin dominate the prey field when they migrate inshore during July to spawn (Davoren, Anderson, & Montevecchi, 2006), essentially transforming the food supply for predators from low during pre-spawning to high during spawning (Davoren, 2013a; Davoren et al., 2006). After inshore arrival but before spawning (early to mid-July), capelin are predominantly observed as small, ephemeral shoals moving northward along the coast (Davoren, 2013a; Davoren et al., 2006). In contrast, spawning capelin aggregations can be predictably located near a cluster of annually persistent deep-water (15e40 m) spawning sites (Gull Island, Fig. 1b; Davoren, 2013a; Penton & Davoren, 2012) located within foraging ranges of seabirds breeding on Funk Island (60e80 km and 60e120 km for murres and gannets, respectively; Burke & Montevecchi, 2009; Garthe et al., 2011). Murres and gannets appear to use both memory-based foraging and local enhancement to locate prey during foraging trips from the colony under these changing prey conditions (Davoren, Montevecchi, & Anderson, 2003a, 2003b, 2010; Garthe et al., 2007, 2011; Montevecchi et al., 2009). Mixed-species feeding assemblages occur within the region (Davoren, 2007, 2013b), typically as large, stable foraging aggregations of seabirds and whales targeting capelin shoals near the seabed. Unlike other regions, common murres target individual capelin separate from or on the periphery of large shoals and do not drive fish schools to the surface (Crook & Davoren, 2014). Thus, mixed-species feeding assemblages associated with concentrations of near-surface fish in this region are rare. Our primary goal was to determine whether seabirds, namely murres and gannets, cue to aggregations of other seabirds to locate potential foraging areas (i.e. local enhancement) during the breeding season on the northeast Newfoundland coast and, if so, whether this strategy becomes less important when prey conditions shift from low biomass, ephemeral shoals to high biomass aggregations that can be predictably located. Using seabird-

(a) 61 59 57 2000 m

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Newfoundland

200m 300m 400m

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Longitude (degrees West) Figure 1. Location of (a) the study area (indicated by the dashed white lines) on the northeast Newfoundland coast and (b) the two experimental decoy sites (i.e. site 1, site 2; black squares), showing annually persistent deep-water spawning sites of capelin (stars) clustered around Gull Island (black circle), and the Funk Island Seabird Ecological Reserve. The greyscale indicates depth contours.

mimicking decoys, we investigated three hypotheses: (H1) breeding seabirds use local enhancement during foraging trips; (H2) use of local enhancement is influenced by the species composition of seabird aggregations; (H3) use of local enhancement is influenced by the presence of predictable prey. If seabirds use local enhancement to cue in on potential foraging areas (H1), we predicted that they would show a higher frequency of responses when decoys were present (treatment periods) relative to when they were absent (control periods). We also predicted that seabirds would respond more to conspecific decoys (H2), given differences in diet and prey capture techniques (pursuit- versus plunge-diving) between gannets and murres. Finally, we predicted that seabirds would use local enhancement to a lesser extent (i.e. decreased responses to decoys) when the prey field shifted to predominantly

K. R. Bairos-Novak et al. / Animal Behaviour 106 (2015) 71e78

persistent shoals of spawning capelin in the study area (H3). Conducting a field-based experiment in a region with known prey behaviour provides an excellent opportunity to understand the foraging strategies used by multiple seabird species to locate prey at sea as well as examine behavioural flexibility as prey conditions change in the foraging environment. METHODS A decoy experiment was conducted during JulyeAugust in 2009 and 2013 on the northeast Newfoundland coast (Fig. 1) when seabird breeding and capelin spawning seasons overlap (Davoren, Penton, Burke, & Montevecchi, 2012). Hatching of most seabirds occurs in mid- to late July and, thus, incubation coincided with experimental days conducted earlier in July, while chick rearing coincided with experimental days later in July. Capelin spawning behaviour differed between years. In 2009, capelin did not spawn at deep-water sites (i.e. only at beach sites; Davoren et al., 2012), resulting in a predominance of ephemeral shoals of capelin throughout the season (Davoren, 2013a). In contrast, spawning occurred at deep-water sites in 2013 and, thus, capelin switched from ephemeral, pre-spawning shoals to persistent, spawning shoals later in July (Davoren, 2013), as is typically observed in most years (Davoren, 2013a; Davoren et al., 2006). During both years, the decoy experiment was conducted along a commuting route of murres and gannets from the Funk Island Seabird Ecological Reserve (site 1, Fig. 1b) to southwestern foraging areas (Davoren et al., 2003a). During capelin spawning in 2013, birds were no longer observed at site 1 and ship-based surveys revealed that murres and gannets shifted commuter routes slightly offshore (Davoren, 2013). Therefore, the decoy experiment was shifted to site 2 (Fig. 1b) for the final 6 experimental days later in July to ensure that the experiment was located on the main seabird commuter route in the study area. Both sites were located in 40e50 m of water and at similar distances from the coast (Fig. 1b). Experimental Design The experimental design involved deploying plastic, painted, floating bird decoys designed to mimic the size and appearance of common murres and northern gannets. Decoys were deployed in different combinations to make up three distinct treatments: ‘Murre’ (N ¼ 75 decoys), ‘Gannet’ (N ¼ 15 decoys) and ‘Hotspot’ (N ¼ 75 murre and N ¼ 15 gannet decoys). These configurations were used to represent typical aggregations and densities in the study area (Davoren, 2007, 2013b). Although floating gannets do not represent actively foraging birds, gannets are often observed sitting in small flocks after bouts of plunge-diving in the study area and, thus, sitting flocks may still indicate nearby prey. At each site, two semipermanent decoy moorings anchored to the sea bed and buoyed by floats were spaced ~100 m apart, with a third mooring located between them and offset approximately 200 m, to anchor the observational platform (i.e. an open boat, 2e3 m long) during control and treatment observation periods. Decoys were attached to each other using cables to create an uneven distribution along each line, again to represent typical murre and gannet flocks in the study area (Davoren et al., 2003a, 2003b). During treatment periods, half of the decoys were placed on each mooring for the Murre and Gannet treatments. In the Hotspot treatment, murre and gannet decoys were attached to separate mooring lines. Treatment periods lasted 30 min with 15 min control periods both before and after each treatment. Decoys were collected and stored under cover aboard the boat during control periods. In 2013, all decoy treatments were conducted each day with treatment order determined randomly through dice roll, whereas in 2009, all treatments were

73

not necessarily conducted each day and therefore treatment order was determined randomly with replacement. Behaviour Observations Although many seabird species were encountered, observations focused on common murres and northern gannets, as they dominate the breeding seabird community in the study area by number and biomass, respectively (Davoren, 2007, 2013b). Atlantic puffins were included in analyses as they were also abundant. Seabirds were observed within a 300 m radius around the boat by a single observer using continuous all-occurrence sampling during control and treatment periods. The observer determined the species, number and behaviour of seabirds, while another individual recorded observations on datasheets. The presence of nearby vessels and marine mammals, along with environmental conditions that could influence observations (e.g. wind direction and speed, sun glare, fog) were also recorded. Seabird behaviours of interest were predetermined to maintain consistency among observers. Eight broad behavioural categories were recorded during treatment and control periods, focusing on the apparent attention of seabirds towards the decoys (Table 1). For pursuit-divers (i.e. murres, puffins), a response was recorded if Circle or Land behaviour was observed (Table 1), as they dive for prey when sitting on the water. For plunge-diving gannets, a response was recorded if Look or Circle was observed (Table 1). Look behaviour could not be reliably recorded for murres and puffins because of the large flock sizes (>100 individuals) as well as the difficulty of observing bill orientation during flight, but this was easier for gannets as their bills were more conspicuous and flock sizes were typically smaller (<20 individuals). Data Analysis Adjacent pre-treatment and post-treatment control periods were combined to compare equal time intervals in control and treatment periods (i.e. 30 min each). During interannual comparisons, only the pre-spawning data (i.e. site 1 in 2013) were included in analyses. Conversely, when comparing between pre-spawning and spawning periods, only 2013 data were included (i.e. site 1 and site 2, respectively). The ‘frequency of response’ was defined as the average number of responses per seabird species during 30 min observation periods. Statistical analyses were conducted using JMP® 10 and R computer programming. The total number of murres, gannets and puffins observed per day within each control or treatment period did not fit a normal distribution (ShapiroeWilk test: murres: W ¼ 0.560, N ¼ 124, P < 0.0001; gannets: W ¼ 0.692, N ¼ 124, P < 0.0001; puffins: W ¼ 0.535, N ¼ 124, P < 0.0001), and could not be corrected using a log transformation (log(x þ 1)). Therefore, to examine whether the number of each of the three seabird species differed among control and treatment periods (H1), treatment types (H2) and periods within years (i.e. pre-spawning, spawning in 2013, H3), we used Wilcoxon two-sample and KruskaleWallis nonparametric tests. Logistic regression was used to examine whether the presence of one or more responses (‘response’) or the absence of responses (‘no response’) of gannets, murres and puffins differed among control and treatment periods (H1), treatment types (H2) and periods within years in 2013 (H3). When significant differences were observed, odds ratios were computed to determine the magnitude of the effect of a parameter on the likelihood of observing seabird responses. When odds ratio tests where statistically significant (i.e. P < 0.05), the 95% confidence intervals did not include 1. To test H2 and H3, we excluded control periods to examine whether the presence/absence of responses during treatment periods differed among treatment types

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Table 1 Description of the eight seabird behaviours examined, indicating which behaviours were characterized as a ‘response’ by pursuit-diving birds (i.e. common murres, Atlantic puffins) and plunge-diving birds (i.e. northern gannets) Behavioural code

Definition

Pursuit-diver response

Plunge-diver response

Fly Look Circle Land Dive Down Dive Up Fight

Flying (without showing any other behaviour described below) Flying with bill pointed 45e90 from the horizon Flying in a semicircular or circular arc Flying and landing on the water Diving into the water from the air (‘pursuit plunging’, sensu Camphuysen & Webb, 1999) Surfacing from a dive Aggressive behaviours involving repeated, close-proximity (<3 m) swooping by one bird towards another while in the air; may or may not involve physical contact Birds present at the observation site at the start of observations or that drifted on the surface into the area during observations

No Noa Yes Yes Nob No No

No Yes Yes Nob Yes No No

No

No

Present a b

Could not be reliably recorded. Not observed or rarely observed (N  2) for a species.

(H2) as well as between pre- and post-spawning periods during 2013 (H3). Using multiple Pearson chi-square tests, we also examined whether the frequency of birds responding differed among control and treatment periods (H1), treatment types (H2) and periods within years (H3), the latter two excluding control period observations. Fisher's exact tests were used when sample sizes were low (N < 5 per cell). We corrected for multiple comparisons using the Benjamini and Hochberg false discovery rate (BH) method. RESULTS A total of 62 control and treatment pairs were conducted in 2009 (N ¼ 27) and 2013 (N ¼ 35). In 2009, experiments were conducted over 11 days during 11 Julye13 August at site 1 and included all three treatments: Murre (N ¼ 8), Gannet (N ¼ 9) and Hotspot (N ¼ 10). In 2013, experiments were conducted at site 1 during capelin pre-spawning over 6 days during 3e10 July (N ¼ 18) and at site 2 during spawning over 6 days during 19e30 July (N ¼ 17) and included all three treatments: Murre (N ¼ 12), Gannet (N ¼ 11) and Hotspot (N ¼ 12). As transit to experiment sites was difficult under extreme weather conditions, most experiments were conducted under low wind (<25 km/h) and sea states (<0.5 m swell height), but a fog bank was present 1e5 km from the coast on ~30% of experimental days (2009: 36%; 2013: 25%), yet, visibility within the observational and surrounding area was not obscured. Preliminary data exploration found no significant trends as a result of fog; therefore, these data were retained in the analysis. On one instance in 2013, visibility within the observational area was drastically reduced (<100 m) and these data were excluded from analysis. Numerical Response to Decoys We observed and recorded 26 212 seabirds in 2009 (8129) and 2013 (18 083). For all species combined, the mean (±SD) number of birds (all species combined) observed per day did not differ between years (2009: 739 ± 780 birds/day; 2013: 1507 ± 1936 birds/ day; Wilcoxon two-sample test: Z ¼ 0.71, P ¼ 0.48), control and treatment periods (Z ¼ 0.095, P ¼ 0.92) or among treatment types (KruskaleWallis test: c22 ¼ 0.048, P ¼ 0.98), but more birds were observed at site 2 (2710 ± 2172 birds/day) than at site 1 (304 ± 224 birds/day; Z ¼ 2.80, P ¼ 0.005) in 2013. For each species, the mean number of birds observed per day did not differ between years (Z  1.65, P  0.099), control and treatment periods (Z  1.78, P  0.075), or treatment types (KruskaleWallis test: c22  1.30, P  0.52). During 2013, significantly more murres and puffins were observed during spawning (i.e. site 2) than during pre-spawning (i.e. site 1; murre: Z ¼ 2.64, P ¼ 0.008; puffin: Z ¼ 2.59, P ¼ 0.008),

but there was no difference between periods for gannets (Z ¼ 0.24, P ¼ 0.81). Behavioural Response to Decoys Species-specific logistic regression models using year and control/treatment periods (treatment types unspecified) were all significant (murre: c22 ¼ 14.84, N ¼ 110, P ¼ 0.001; puffin: c22 ¼ 8.20, N ¼ 89, P ¼ 0.017; gannet: c22 ¼ 47.71, N ¼ 109, P < 0.0001). The likelihood of birds responding did not differ between years for murres (c21 ¼ 1.40, P ¼ 0.24) or puffins (c21 ¼ 0.03, P ¼ 0.86), but did for gannets (c21 ¼ 15.33, P < 0.0001), with responses to decoys being 10.51 times more likely in 2013 compared to 2009 (odds ratio c21 ¼ 20.87, P < 0.0001). Birds were more likely to respond (i.e. presence of one or more responses) when decoys were present (i.e. treatment) than when absent (i.e. control; H1) for all species (murre: c21 ¼ 12.69, P ¼ 0.0004; puffin: c21 ¼ 6.00, P ¼ 0.014; gannet: c21 ¼ 22.65, P < 0.0001; Fig. 2a). Indeed, the presence of decoys was 4.32 times more likely to elicit at least one response in murres (odds ratio c21 ¼ 13.59, P ¼ 0.0002; Fig. 2), 7.14 times more likely in puffins (odds ratio c21 ¼ 8.13, P ¼ 0.0044; Fig. 2) and 16.57 times more likely in gannets (odds ratio c21 ¼ 33.30, P < 0.0001; Fig. 2a). Similarly, more birds responded within treatment relative to control periods for murres (c21 ¼ 83.6, P < 0.0001; BH correction: a0 ¼ 0.0042), puffins (c21 ¼ 10.68, P ¼ 0.001, a0 ¼ 0.021) and gannets (c21 ¼ 168.8, P < 0.0001, a0 ¼ 0.0042; Fig. 2b). Species-specific logistic regression models excluding control periods (i.e. treatment type as main factor) revealed that the likelihood of the presence of one or more responses did not differ among treatment types (H2) for murres (c22 ¼ 4.47, N ¼ 55, P ¼ 0.11), puffins (c22 ¼ 3.46, N ¼ 44, P ¼ 0.18), or gannets (c22 ¼ 5.91, N ¼ 56, P ¼ 0.052; Fig. 3a). The frequency of puffins responding did not differ between treatment types (Fisher's exact test: P ¼ 0.10; Fig. 3b), but did for murres (c22 ¼ 9.51, P ¼ 0.009, a0 ¼ 0.029), with more murres responding to the Murre treatment relative to the Gannet treatment (c21 ¼ 8.68, P ¼ 0.003) and the Hotspot relative to the Gannet treatment (c21 ¼ 6.93, P ¼ 0.009; Fig. 3b). Similarly, the proportion of gannets responding differed between treatment types (c22 ¼ 6.90, P ¼ 0.032; a0 ¼ 0.033), with more gannets responding to the Hotspot treatment relative to the Murre treatment (c21 ¼ 6.40, P ¼ 0.011; Fig. 3b). During 2013, the likelihood of the presence of one or more responses did not differ between pre-spawning (i.e. site 1) relative to spawning (i.e. site 2; H3; control periods and 2009 data excluded) for murres (c21 ¼ 0.068, N ¼ 30, P ¼ 0.79), puffins (c21 ¼ 0.40, N ¼ 23, P ¼ 0.53) or gannets (c21 ¼ 1.05, N ¼ 33, P ¼ 0.31; Fig. 4a). The frequency of birds responding did not differ between both periods for puffins (Fisher's exact test: P ¼ 0.25) or gannets

K. R. Bairos-Novak et al. / Animal Behaviour 106 (2015) 71e78

1

1

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*

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Proportion of periods with bird responses

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75

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Figure 2. Proportion of (a) control (black bars) and treatment (white bars) pairs with one or more responses and (b) total birds observed responding within control and treatment periods by common murres, Atlantic puffins and northern gannets. Number of responses observed are indicated in parentheses. *P < 0.05.

(c21 ¼ 0.43, P ¼ 0.84), but more murres responded during prespawning relative to spawning (c21 ¼ 510.5, P < 0.0001, a0 ¼ 0.0042; Fig. 4b). General Observations Out of all murres that responded to the decoys (i.e. Circle, Land; Table 1), most murres landed within the decoys (63%), while 37% circled over the decoys and did not land. In contrast, puffins responded primarily by circling the decoys (68%) and fewer landed (32%). Murres sitting among the decoys often vocalized and dipped their head in the water, presumably looking for prey. Of the gannets responding (i.e. Look, Circle, Dive Down; Table 1), most circled (63%), while fewer were observed looking (36%) and plunge-diving

0

Murres

(12) (4) (18) Puffins

Gannets

Species Figure 3. Proportion of (a) each treatment type (Murre: black bars; Gannet: white bars; Hotspot: grey bars) with one or more responses and (b) total birds observed responding within each treatment type for common murres, Atlantic puffins and northern gannets. Number of responses observed are indicated in parentheses. Bars not sharing the same letter differed significantly (*P < 0.05).

(1%) near the decoys. When circling, gannets first flew directly over the decoys with their beaks facing towards the decoys (Look; Table 1), followed by a tightly knit figure-eight circling pattern directly over the decoys and then a larger figure-eight pattern over a broader area adjacent to the decoys. Although gannets primarily circled the decoys as solitary individuals, aggregations of 4e10 circling gannets were observed on three separate occasions during the Hotspot (N ¼ 2) and Gannet (N ¼ 1) treatments at site 1 (prespawning) in 2013 under overcast and foggy conditions. During each of these events, one or two gannets broke off from a flying flock and began circling the decoys (described above), and then more gannets joined from other passing flocks.

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1

Proportion of periods with bird responses

(a)

0.8

0.6 (15) (14)

0.4 (9)

(11)

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Murres

Puffins Species

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Proportion of birds responding

(b)

0.3

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(134) (68)

0.1 (37) (2) (42) 0

Murres

(6) Puffins Species

Gannets

Figure 4. Proportion of (a) each prey period (pre-spawning, site 1: black bars; spawning, site 2: white bars) with one or more responses and (b) total birds observed responding within each prey period for common murres, Atlantic puffins and northern gannets. Number of responses observed are indicated in parentheses.*P < 0.05.

DISCUSSION Seabirds altered their behaviour in the presence of decoys, with birds being 4e17 times more likely to respond and proportionately more birds responding during treatment relative to control periods. Although we cannot rule out that seabirds were attracted merely to floating objects, preference for conspecific decoys suggests some recognition of decoys as seabirds, thereby providing support for our first hypothesis (H1), that all three species use local enhancement within the study area. The species composition of decoys influenced murre and gannet responses, with both species relying to a greater extent on information from conspecifics than from allospecifics (H2). Specifically, murres responded more to the Murre

and Hotspot treatments relative to the Gannet treatment, and gannets responded more to the Hotspot than Murre treatment. Although puffins tended to respond more to pursuit-divers (i.e. murres) relative to plunge-divers (i.e. gannet), puffin responses were not significantly influenced by decoy species composition, possibly due to the absence of conspecific decoys. Murres responded proportionally more to decoys during pre-spawning (site 1) relative to spawning (site 2) in 2013, suggesting that murres use local enhancement to a lesser extent when prey can be predictably located (H3). Although seabirds altered their behaviour, seabird abundance did not change when decoys were present, but abundance was significantly higher during spawning at site 2 relative to prespawning at site 1. The latter was not surprising because seabird densities are typically higher along the coast during spawning relative to pre- and post-spawning (Davoren, 2007, 2013b). Similar seabird abundances when decoys were present and absent, however, suggest that birds responded to decoys when flying in close proximity (~1 km) but that they were not recruited from farther away. Although theoretical visual detection distances of feeding flocks by seabirds range between 20 km and 30 km, observed distances are estimated to be <10 km, with a mean of ~4.5 km (Haney, Fristrup, & Lee, 1992). In another study, flying gannets had low reaction distances (~0.5e6 km) when cueing to small flocks (<10 birds) of conspecifics sitting on the water (Thiebault, Mullers, Pistorius, & Tremblay, 2014), similar to the flock sizes and behaviour of our Gannet treatment. Although flock sizes were much higher in the Murre (N ¼ 75) and Hotspot (N ¼ 75 murres and N ¼ 15 gannets) treatments relative to the Gannet treatment (N ¼ 15), the inconspicuous counter-shading plumage of murres would not likely increase detection ranges (Hoffman et al., 1981). In addition, fog banks were observed 1e5 km offshore of the experimental site on approximately one-third of experimental days, which would limit detection ranges and reduce the probability of a numerical response by seabirds. Responses of all three seabird species to the decoys adds to the mounting evidence of marine predators using public information to locate prey. Evidence suggests that local enhancement is a beneficial strategy, including widespread reports of multispecies feeding assemblages of seabirds with conspecifics and other predators as well as the attraction of seabirds to these assemblages (e.g. Camphuysen & Webb, 1999; Harrison et al., 1991; Hoffman et al., 1981; Porter & Sealy, 1981) and responses to other predators at sea during experiments (e.g. Haney et al., 1992; Porter & Sealy, 1982; this study). Indeed, modelling (e.g. Grunbaum & Veit, 2003) as well as observational studies (e.g. Thiebault, Mullers, Pistorius, & Meza-Torres et al., 2014, Thiebault, Mullers, Pistorius, & Tremblay, 2014; Tremblay et al., 2014) indicate that seabirds have higher foraging success and/or expend less time/energy while searching if public information is used. For instance, cape gannets, Morus capensis, halve the time to first dive on foraging trips from the colony during the breeding season by responding to flying conspecifics either returning to or departing from the colony (Thiebault, Mullers, Pistorius, & Meza-Torres et al., 2014). The degree to which local enhancement is used depends on how reliably the cue (i.e. foraging activity of other predators) indicates patches of accessible and preferred prey types. In this study, murres and gannets responded more to conspecifics, or in the case of puffins, to species within the same foraging guild (i.e. pursuitdivers). Despite overlap in foraging areas and diets of murres, puffins and gannets in the study area (Davoren, 2013b), puffins and gannets rely to a greater extent on other prey species (Bennett, Burke, Hedd, & Montevecchi, 2013; Burke & Montevecchi, 2008) than do murres (Davoren & Montevecchi, 2003) and access capelin at different depths (e.g. gannets: <22 m, Garthe, Benvenuti, &

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Montevecchi, 2000; murres: <150 m, Hedd et al., 2009). Therefore, conspecifics may provide the most reliable cues when searching for prey. Indeed, gannets are typically associated with conspecifics and/or marine mammals (e.g. dolphins, whales) in the study area (Davoren et al., 2010) and elsewhere (e.g. Camphuysen & Webb, 1999; Thiebault, Mullers, Pistorius, & Tremblay, 2014; Tremblay et al., 2014). Gannets did not respond more to the Gannet treatment relative to the Hotspot treatment, however, possibly because sitting, nonforaging gannet decoys alone may not reliably signal nearby prey. Although pursuit-divers are considered ‘initiators’ of mixed-species feeding assemblages in other regions (Hoffman et al., 1981), this is unlikely in our study area. Capelin are associated with the sea bed (Davoren et al., 2006), and murres typically attack solitary capelin from above at capelin spawning sites (Crook & Davoren, 2014), thereby likely driving prey deeper in the water column. Gannet diets also include larger pelagic fish (e.g. herring, salmon) when available in the study area (Montevecchi, 2007) and, thus, capelin are considered a ‘default prey’ when these other fish are not present. Overall, this suggests that foraging activities of pursuit-divers alone would primarily indicate to gannets the location of dispersed, less accessible and less desired prey. For similar reasons, gannets probably do not provide a reliable cue of profitable foraging areas for pursuit-divers. As plunge-divers, gannets may further disrupt underwater prey location and capture by pursuitdivers if foraging together on a fine-scale (Hoffman et al., 1981). Indeed, the greater response of murres (and puffins) to large aggregations of murres (Murre, Hotspot), but not to gannets alone (Gannet) supports this contention. Despite responding more to conspecifics during single-species treatments (i.e. Murre, Gannet), all species responded similarly (i.e. murres, puffins) or more (i.e. gannets) to the Hotspot treatment, suggesting that they respond more to a higher bird density regardless of whether allospecifics are present. As seabirds in the study area are typically observed in mixed-species assemblages with no coordinated feeding activities (i.e. type II mixed-species feeding assemblages; Camphuysen & Webb, 1999), a higher response to the Hotspot treatment was not surprising. The relative costs and benefits of local enhancement in relation to other search strategies are also likely to influence the use of public information to locate prey. Pursuit-divers were less likely to use local enhancement (~4e7 times) than gannets (~17 times), and fewer murres responded to decoys when capelin could be predictably located. This suggests that local enhancement is less profitable for murres than other strategies, such as memory, during capelin spawning (Davoren et al., 2003a). Additional evidence for this shows that murres are the primary species found in high abundance at predictable aggregations of capelin (Davoren, 2013b) and show tight associations with capelin (Davoren et al., 2003b). As local enhancement presumably involves more flying and landings on the water than does flying directly to a remembered location (i.e. memory), switching to memory may be of critical importance for murres because of their extremely high costs of flight (Elliott et al., 2013) as well as generally high costs of landing on and taking off from the water (e.g. Shaffer, Costa, & Weimerskirch, 2001). In contrast, our findings suggest that local enhancement may be more profitable for gannets, as they have lower flight costs and they prey on a variety of species, all of which cannot be predictably located. Gannets are also less associated with deep-water spawning sites of capelin than are murres (Davoren, 2013b) and are more tightly associated with baleen whales than with capelin in the study area (Davoren et al., 2010), consistent with local enhancement being more profitable. However, local enhancement may be less profitable when prey become limited due to increased competition, as gannets were less likely to respond to decoys in 2009, when capelin biomass was an order of magnitude lower (~0.008 g/m2) than in

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other years in the study area (0.03e0.06 g/m2; Downs, 2013). Therefore, gannets may also use other search tactics, such as arearestricted search, to further concentrate search effort where prey is most likely to be encountered (Einoder et al., 2011; Hamer et al., 2009). For example, the circling behaviour of gannets near decoys was similar to that described as area-restricted search, characterized by a decrease in travel speed and an increase in turning rate (Paiva et al., 2010). Although seabird species relied on local enhancement to varying degrees, possibly owing to varying dietary preferences and flight costs, this study provides further support for the importance of local enhancement as a strategy that marine predators use to locate ephemeral prey at sea even under varying levels of capelin biomass within and between years. This suggests that competition among predators will not be important unless prey density in the study area becomes extremely low (Tremblay et al., 2014). In contrast, densities of predators above a particular threshold, specifically conspecifics, may be required for efficient foraging (Grunbaum & Veit, 2003; Tremblay et al., 2014), suggesting that Allee effects may be observed at the population level when predator densities drop below this threshold.

Acknowledgments Principal funding was provided by Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery (28321207) and Ship Time (372594-09, 436824-2013) grants, along with International Polar Year and University of Manitoba Research Grants Program and Faculty of Science Fieldwork Support Program grants to G.K.D. K.A.C. was funded by a University of Manitoba Faculty of Science Undergraduate Student Research Award (USRA) and K.B.N. was funded by a NSERC USRA. Special thanks to Larry Easton and crew aboard the Lady Easton and Lady Easton II and well as Dan Goodyear and Darren Hillier, without whom this study would not have been possible. Thanks to J. Allen, E. Maxner, L. Hayhurst, K. Downs, D. Jameson, L. Jameson and M. Mai for assistance with field work. References Bayer, R. D. (1983). Black-legged kittiwake feeding flocks in Alaska: selfish/reciprocal altruistic flocks? Journal of Field Ornithology, 54, 196e199. Bennett, S. G., Burke, C. M., Hedd, A., & Montevecchi, W. A. (2013). Comparison of capelin Mallotus villosus in the prey loads of common murres Uria aalge and northern gannets Morus bassanus foraging from the same breeding site in the Northwest Atlantic. Marine Ornithology, 41, 179e182. Burke, C. M., & Montevecchi, W. A. (2008). Fish and chicks: forage fish and chick success in co-existing auks. Waterbirds, 31(3), 372e384. Burke, C. M., & Montevecchi, W. A. (2009). The foraging decisions of a central place foraging seabird in response to fluctuations in local prey conditions. Journal of Zoology, 278, 354e361. Camphuysen, C. J., & Webb, A. (1999). Multi-species feeding associations in North Sea seabirds: jointly exploiting a patchy environment. Ardea, 87, 177e198. Carscadden, J. E., & Vilhjalmsson, H. (2002). Capelin: what are they good for? ICES Journal of Marine Science, 59, 863e869. Clapham, P. J., Baraff, L. F., Carlson, C. A., Christian, M. A., Matilla, D. K., Mayo, C. A., et al. (1993). Seasonal occurrence and annual return of humpback whales, Megaptera novaeangliae, in the southern Gulf of Maine. Canadian Journal of Zoology, 71, 440e443. Crook, K. A., & Davoren, G. K. (2014). Underwater behaviour of common murres foraging on capelin: influences of prey density and antipredator behaviour. Marine Ecology Progress Series, 501, 279e290. Dall, S. R. X., Giraldeau, L.-A., Olsson, O., McNamara, J. M., & Stephens, D. W. (2005). Information and its use by animals in evolutionary ecology. Trends in Ecology & Evolution, 20(4), 187e193. Davoren, G. K. (2007). The spatial and temporal overlap of a biological hotspot and fishing activities: negative humanewildlife interactions in the Northwest Atlantic. Conservation Biology, 21, 1032e1045. Davoren, G. K. (2013). [At-sea surveys with simultaneous recordings of seabird and capelin density and distribution conducted in association with the present study]. Unpublished raw data.

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