Stewart Et Al. 2013

Deep-Sea Research II 95 (2013) 197–208

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Deep-Sea Research II

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Behavioral ecology of jumbo squid (Dosidicus gigas) in relation to oxygen minimum zones

Julia S. Stewart a,n, John C. Field b, Unai Markaida c, William F. Gilly a a Hopkins Marine Station, Stanford University, 120 Oceanview Boulevard, Paciﬁc Grove, CA 93953, USA b Fisheries Ecology Division, SWFSC/NMFS/NOAA, 110 Shaffer Road, Santa Cruz, CA 95060, USA c Pesquerı´as Artesanales, El Colegio de la Frontera Sur, CONACyT, Avda. Rancho Polı´gono 2A, Cuidad Industrial Lerma, 24500 Campeche, Mexico article info abstract

Available online 28 June 2012 Habitat utilization, behavior and food habits of the jumbo or Humboldt squid, Dosidicus gigas,were Keywords: compared between an area recently inhabited in the northern California Current System (CCS) and a Deep scattering layer historically established area of residence in the Gulf of California (GOC). Low dissolved oxygen Diel vertical migration concentrations at midwater depths deﬁne the oxygen minimum zone (OMZ), an important environmental Diet feature in both areas. We analyzed vertical diving behavior and diet of D. gigas and hydrographic Diving properties of the water column to ascertain the extent to which squid utilized the OMZ in the two areas. Humboldt squid The upper boundary of the OMZ has been shoaling in recent decades in the CCS, and this phenomenon has Hypoxia been proposed to vertically compress the pelagic environment inhabited by aerobic predators. A shoaling Oxygen minimum zone OMZ will also bring mesopelagic communities into a depth range with more illumination during daytime, Range expansion making these organisms more vulnerable to predation by visual predators (i.e. jumbo squid). Because the Satellite tagging OMZ in the GOC is considerably shallower than in the CCS, our study provides insight into the behavioral plasticity of jumbo squid and how they may respond to a shoaling OMZ in the CCS. We propose that shoaling OMZs are likely to be favorable to jumbo squid and could be a key indirect factor behind the recent range expansion of this highly migratory predator. & 2012 Elsevier Ltd. All rights reserved.

1. Introduction except several years associated with El Ninõevents(Gilly and Markaida, 2010; Markaida, 2006). During the last decade jumbo squid (also called Humboldt squid, Pop-up archival transmitting (PAT) satellite tags have been Dosidicus gigas) have been undergoing a major range expansion in successfully deployed and recovered in the assessment of rela- the eastern Pacific Ocean, where they are endemic. This species tively short-term (o1 month) patterns of vertical movement and generally inhabits areas beyond the continental shelf but is well habitat use of jumbo squid in the GOC (Gilly et al., 2006) and the known for transient excursions into shallower coastal waters that Pacific coast of Baja California (Bazzino et al., 2010). These studies often result in mass strandings. Jumbo squid are large, highly have revealed general patterns in vertical migration. Daytime is migratory, and effective visual predators capable of tolerating large typically spent in the midwater environment with shallower and rapid changes in environmental conditions, including pressure, depths occupied at nighttime, but rapid migrations throughout temperature and dissolved oxygen concentration (Gilly et al., 2006). the water column can occur at any time. Understanding the behavior of such predators and their ecosystem In the eastern tropical Pacific (Nigmatullin et al., 2001), as well as interactions, particularly in conjunction with climate change, has in the northern CCS (Field et al., 2007, 2013), the GOC (Markaida and been of great interest to ecologists, fisheries scientists and commer- Sosa-Nishizaki, 2003) and off the Pacific coast of Baja California cial fishing operators. Studies concerning horizontal movements and (Bazzino et al., 2010), jumbo squid feed primarily on small meso- diet have occurred in the northern California Current System (CCS) pelagic fishes, squids, and crustaceans that are components of the during this range expansion (Field et al., 2007, 2013; Zeidberg and acoustic deep scattering layer (DSL). However, in the northern CCS, Robison, 2007) as well as in the central Gulf of California (GOC) (Gilly significant predation also occurs on a variety of much larger fishes of et al., 2006; Markaida and Sosa-Nishizaki, 2003; Markaida et al., considerable ecological and commercial importance, including Paci- 2005, 2008), where jumbo squid have occurred in commercial fic hake (Merluccius productus), several species of rockfish (Sebastes quantity year-round since the mid 1990s (Markaida et al., 2005) spp.), many flatfish species (Pleuronectidae) (Field et al., 2007)and even salmonids (Braid et al., 2012; Field et al., 2013). The eastern Pacific Ocean is characterized by the world’s

n Corresponding author. Tel.: þ1 831 655 6220; fax: þ1 831 375 0793. largest and shallowest oxygen minimum zone (OMZ) (Keeling E-mail address: [email protected] (J.S. Stewart). et al., 2010), a midwater region where the dissolved oxygen (DO)

0967-0645/$ - see front matter & 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.dsr2.2012.06.005 198 J.S. Stewart et al. / Deep-Sea Research II 95 (2013) 197–208 concentration is r20 mmol/kg, or 0.5 mL/L (Fig. 1; Helly and that clearly utilizes the upper OMZ in the GOC and likely uses this Levin, 2004). Several recent studies have indicated an ongoing environmental feature in conjunction with both foraging on meso- expansion of the OMZ, primarily through shoaling, throughout pelagic organisms and predator avoidance (Davis et al., 2007; Gilly the eastern Pacific (Bograd et al., 2008, 2010; Stramma et al., et al., 2006). This is also the case in the northern CCS, but squid in 2008; Whitney et al., 2007), and scenarios of the climate change this region utilize the continental shelf environment to a much suggest a continuation of this trend in the future (Deutsch et al., greater extent. We find that jumbo squid can tolerate cold, hypoxic 2011; Keeling et al., 2010). conditions for long periods, perhaps longer than most, if not all, Shoaling of midwater hypoxic regions in the Atlantic Ocean large pelagic competitors and predators. They can also make rapid has been shown to cause vertical habitat compression of the well deep dives across the OMZ to depths of 41200 m, probably as an oxygenated, upper water column inhabited by predatory fishes escape mechanism from some of those predators. Shoaling of the and may result in an increased susceptibility to commercial upper OMZ could thus uniquely favor jumbo squid, and we propose fishing pressure (Prince and Goodyear, 2006; Prince et al., 2010; that this changing midwater feature is an important indirect factor Stramma et al., 2011). Although DO in these regions is consider- behind the recent range expansion of this species in the northern ably higher than that in the Pacific OMZ, the effects of a shoaling hemisphere. hypoxic front are likely to be similar in both areas. Another potential effect of a shoaling OMZ in the Pacific is the transloca- tion of mesopelagic communities that inhabit the upper OMZ to 2. Methods shallower, more illuminated depths, and this could make these mesopelagic organisms more susceptible to visual predators 2.1. Vertical habitat and behavior (Koslow et al., 2011). Clearly there are multiple and interacting effects expected for 2.1.1. Tagging pelagic predators in association with OMZ shoaling, and not all All squid in this study were collected with weighted lumines- predators are likely to be affected in the same ways. Jumbo squid cent jigs (0.35 m) using rod and reel or hand-line, carefully forage largely on the mesopelagic micronekton that comprise the brought onboard the vessel by lifting the jig with a heavy DSL, and because they are visual predators that can tolerate cold, monofilament leader, and tagged on the ventral side of the fin low oxygen conditions (Gilly et al., 2006), they might be favored as close to the gladius as possible with Mk10 pop-up archival relative to other pelagic predators by a shoaling OMZ. transmitting tags (PAT: Wildlife Computers, Redmond, Washing- This study provides insight concerning the question of how a ton, USA). Previously described tagging procedures (Gilly et al., shoaling OMZ may affect jumbo squid, a highly migratory predator. 2006) were modified in 2006, mainly by securing the tag to a We tagged large squid off central California in the CCS and analyzed small plastic platform (from which it released) that was attached their diving behavior and vertical habitat use in relation to the OMZ to the squid’s fin by two nylon bolts (1/4-20) and secured with (r20 mmol/kg DO) and the hypoxic region above it (20–60 mmol/ nylon washers and nuts. Squid in the CCS were tagged in autumn kg DO). Because models predict a continued shoaling of the OMZ in (2008–2009), and squid in the GOC were tagged in the Guaymas this region, we reanalyzed existing jumbo squid tag data from the Basin during spring and autumn (2004–2008). Tags were pro- Guaymas Basin in the GOC, a region where the OMZ is much grammed to record temperature (resolution of 0.05 1C) and shallower and perhaps similar to the future scenario for the CCS. In pressure (depth resolution of 0.5 m) at 1 Hz, and a full record of both regions, we also compared new and existing food habits data archived data was available upon recovery of the tag. CCS tags in to infer differences in foraging behavior. Dosidicus gigas is a species 2009 were able to upload a 0.01 Hz subsampled record to Argos,

Fig. 1. Dissolved oxygen at 300 m in the Pacific Ocean with the approximate range of jumbo squid (white curve). The recent range expansion at the northern limit is shown shaded in transparent white. Dissolved oxygen data and map are from the World Ocean Atlas Database (www.nodc.noaa.gov/OC5/WOA01F/prwoa01f.html). Focus regions in this study are boxed: the CCS in red and the GOC in yellow. Detailed maps of tagging locations are published elsewhere (Stewart et al., in review; Gilly et al., 2006; in press). J.S. Stewart et al. / Deep-Sea Research II 95 (2013) 197–208 199 and these data were used if the tag was not recovered. As we were Polynomials were 2nd–5th order, depending on the shape and interested in characterizing diving behavior and vertical veloci- depth of the profile, and the final equation was chosen based on ties, only data from recovered tags or those that delivered time- smallest root-mean-square difference between the data and the series data through Argos (CCS tags deployed after 2008) were calculated curve (Fig. 2). This equation was then used to estimate analyzed in conjunction with this study. Methods for active DO concentrations at depths sampled by the tags, which, along recovery of tags at sea are described elsewhere (Gilly et al., in with the depths and corresponding temperatures, were used to press). describe the midwater habitat of D. gigas. The polynomials tended Five of the nine tags deployed in CCS and six of the nine tags not to fit oxygen profiles near the surface well, and depths recovered in the GOC yielded useful time-series data for a total of o15 m were therefore not included in analyses involving oxygen. 35.0 days and 57.2 days in the two respective locations (Table 1). Because there is discussion around what defines hypoxia for Deployments ranged from 2.7 to 17.6 days, and tags were marine organisms (Hofmann et al., 2011; Vaquer-Sunyer and programmed for short periods (17 days–1 month) based on Duarte, 2008), two oxygen concentration ranges were specifically experience from previous studies (Bazzino et al., 2010; Gilly identified in our analyses: the oxygen minimum zone (OMZ), et al., 2006). Naming of CCS tags is consistent with other reports defined as r20 mmol/kg DO, and what we call the oxygen limited (Stewart et al., in review), and a similar naming scheme for GOC zone (OLZ) defined as the region with DO concentrations of 20– tags was followed. 60 mmol/kg.

2.1.2. Environmental data 2.1.3. Analysis We assessed dissolved oxygen concentration (DO) and other Diving behavior was analyzed by subsampling archival time- properties of the water column in the area of tag deployments series data (1 Hz sampling) to 0.01 Hz to be consistent with low- with independent hydrographic measurements. In the CCS, rele- resolution time-series data uploaded to Argos from CCS tags vant environmental data were accessed through an internal deployed in 2009. Tags were analyzed individually and grouped database at the Monterey Bay Aquarium Research Institute by location, and summary values are reported as both mean (MBARI) by S. Haddock. Stored environmental data had been (7SD) and median values in Table 2, because the data are often sampled using a Seabird SBE19plus conductivity–temperature– not normally distributed. Analyses of squid association with the depth (CTD) profiler equipped with a Seabird SBE43 DO sensor OMZ are based on depths of 415 m as discussed in Section 2.1.2 (Seabird Electronics, www.seabird.com). The CTD-O profiler was and the first three days of deployment only. We imposed this attached to remotely operated vehicles (ROVs) and sampled temporal restriction because D. gigas is highly migratory (Gilly continuously during dives. Twelve of these CTD-O profiles sam- et al., 2006; Markaida et al., 2005) and could have left the area pling up to 2480 m deep within one month of tag deployment from which oxygen profiles were available. (Nov–Dec 2009) in the area of tag deployments (36–36.751N) Average velocities during vertical migrations were analyzed by were used to characterize DO concentration throughout the water setting a window of 730 min around the times for sunrise and column in the CCS. In the GOC, the same parameters were sunset at the deployment location, and an average rate of move- measured to a maximum depth of 600 m at the time of tag ment was calculated between the depths defined by these two deployment using a Seabird SBE19plus profiler and SBE-43 oxy- time points. A similar procedure was used for deep dives by gen sensor (Gilly et al., 2006). In addition, a single DO profile to choosing two points in time where the squid entered and exited 1500 m using a SBE-43 oxygen sensor was made from the R/V the OMZ. New Horizon in June 2011, and these data were spliced together All analyses were performed using original scripts made in with oxygen data from the profiles to 600 m. This procedure was MATLAB 7.9.0 (The Mathworks, Natick, Massachusetts, USA). necessary to estimate the DO concentration experienced by squid making dives 4600 m in the GOC. As DO in the GOC is generally 2.2. Diet o5 mmol/kg below 600 m, any error introduced by this procedure was negligible. In order to compare diet composition with tagging data, we In both locations, mean profiles for DO were computed based reanalyzed available food habits data from the appropriate on casts corresponding to specific groups of tags (see Table 2) and regions that overlapped with tagging data. Samples in the CCS fitted with a polynomial using the polyfit function in MATLAB. were taken from 2005 to 2006 (n¼775) off central and southern

Table 1 Deployment and popup information for the CCS and GOC. All GOC tags and CCS-1 and CCS-6 were recovered. CCS-6 did not pop-up and report its position to Argos, but it was opportunistically recovered on a beach in Maui, Hawaii 1.5 years after deployment.

Squid TagID DML (m) Deployment Pop-up Sampling time (d)

Date Position Date Position

1N 1W 1N 1W

CCS autumn CCS-1 83046 0.68 10/12/08 37.91 123.48 10/15/08 37.65 123.99 2.7 CCS-3 83052 0.67 11/05/09 36.59 122.06 11/12/09 36.23 123.30 5.7 CCS-4 64004 0.69 11/05/09 36.58 122.05 11/10/09 36.18 122.09 3.0 CCS-5 83051 0.79 11/05/09 36.58 122.06 11/24/09 32.09 118.45 17.6 CCS-6 83048 0.79 12/4/09 36.69 122.05 – – – 6.0

GOC spring GOC-2 62007 0.70 3/13/07 27.95 111.22 3/19/07 27.08 111.15 3.5 GOC-3 62009 0.75 3/13/07 27.95 111.22 3/29/07 26.59 109.87 15.2 GOC-5 64006 0.80 5/4/08 27.34 112.32 5/16/08 28.62 112.12 8.3

GOC autumn GOC-1 52869 0.83 10/25/04 27.34 112.22 11/2/04 27.43 111.01 8.0 GOC-4 64004 0.77 11/16/08 27.53 112.32 11/30/08 27.64 111.27 12.0 GOC-6 83048 0.79 11/16/08 27.53 112.32 11/28/08 28.62 112.115 10.2 200 J.S. Stewart et al. / Deep-Sea Research II 95 (2013) 197–208 8.6 [30.8] 13.2 [26.9] 18.1 [24.0] 8.8 [27.6] 7 77 7 7 21.6 [4.6] 25.3 5.9 [33.7] 31.9 18.1 [32.2] 28.6 7.0 [7.5] 31.6 mol/kg) are reported as percent of 7 7 7 7 m OMZ (%) OLZ (%) 22.3 [44.2] 6.6 50.6 [42.9] 14.7 19.5 [17.1] 35.4 41.5 [26.4] 25.1 7 7 7 7 (umol/kg) C) Oxygen 1 1.6 [7.6] 44.9 2.3 [12.1] 53.4 2.0 [12.0] 25.6 2.2 [12.1] 40.2 7 7 7 7

Fig. 2. Oxygen-depth data used to derive dissolved oxygen concentration from

mol/kg) and oxygen limited zone (OLZ, 20–60 tag-sampled depth data: an example for CCS tags. Light gray circles represent raw m data from twelve CTD-O casts conducted by MBARI between November 16 and 20 December 14, 2009 in the tagging area, and larger black circles are the mean SD [median] depths and temperatures are from tagged squid, and oxygen data for each r 189.6 [334.0] 7.7 153.2 [239.5] 12.6 121.6 [270.5] 12.3 139.4 [255.7] 12.5

7 oxygen values at 1-m depth bins. The thick black line shows the ﬁtted polynomial 7 7 7 7 for depths 415 m (root mean squares¼2.39): y¼2.4e12x4–1.1e8 3þ 1.9e5x2–1.4e2xþ4.0. The dashed line indicates 20 mmol/kg DO (upper boundary of the OMZ), and the dotted-dashed line indicates 60 mmol/kg DO (the upper boundary of a hypoxic region we call the oxygen limited zone or OLZ). 45.6 [145.7] 363.2 87.6 [125.6] 229.8 37.6 [68.2] 268.2 68.7 [76.8] 249.2 California (35–381N) (Field et al., 2007, 2013). Samples were 7 7 7 7 taken in the GOC from 1995 to 1997 (n¼235), 1999 to 2000 (n¼203) and 2005 to 2007 (n¼150) in the Guaymas Basin, with 403 samples off Santa Rosalia and 185 off Guaymas (27–281N) (Markaida and Sosa-Nishizaki, 2003; Markaida, 2006; Markaida C) Oxygen (umol/kg) Depth (m) Temp ( 1 2.6 [12.1] 122.2 3.1 [18.5] 114.3 3.8 [18.1] 66.9 3.5 [18.3] 87.7 et al., 2008). Stomachs from jumbo squid caught individually 7 7 7 7 using jigs were frozen for analysis in the laboratory as described elsewhere (Field et al., 2007; Markaida et al., 2008). Prey were identiﬁed visually by undigested hard parts (otoliths, bones, beaks), enumerated and assigned to the lowest taxonomic resolution possible, except crustaceans and pteropods, which were too 167.1 [44.5] 11.7 76.1 [27.5] 17.5 142.1 [83.0] 17.5 122.0 [59.6] 17.5 fragmented to be counted accurately. Prey size was estimated 7 7 7 7 from hard part dimensions when possible.

Depth (m) Temp ( Diet composition was assessed with squid of a much greater

Nightn size range Day compared with tagged squid that were Percent of time all very large (Table 1). The large differences in sizes of both D. gigas and prey across locations were addressed by comparing the percent frequency of occurrence (%FO), percent of total number (%N) and 32.4 [256.9] 5 107.8 46.5 [182.6] 3 62.9 10.4 [94.4] 3 125.7 58.7 [97.6] 8 98.3 estimated sizes of different prey items normalized by the size of 7 7 7 7 the predator (Field et al., 2007; Markaida, 2006; Markaida et al., 2008). Prey were grouped into coarse taxonomic categories to facilitate a broad comparison of prey components. 40.3 [484.5] 252.8 62.5 [204.7] 207.3 24.4 [237.0] 98.6 52.5 [209.7] 135.3 3. Results 7 7 7 7

in terms of depth, temperature and dissolved oxygen in the CCS and the GOC. Daytime and nighttime mean 3.1. Vertical distribution and behavior OMZ depth (m) OLZ depth (m) 3 236.9 3 232.7 5 235.5 n CTD Tags 12 495.0 Jumbo squid tagged in this study were among the largest encountered in each area, ranging from 0.67 to 0.79 m mantle

Dosidicus gigas length (ML) in the CCS and from 0.70 to 0.83 m ML in the GOC. All tagged squid in both locations exhibited a diel pattern of vertical

(all) migration from midwater depths during the day to shallower Location and season CCS autumn GOC spring GOC autumn GOC all the individual tag deployments. All oxygen calculations are for the ﬁrst three days of deployment as described in the text. Table 2 Habitat of squid are derived from CTD casts. Large standard deviations are indicative of deep dives. Occupancy in the oxygen minimum layer (OMZ, depths at night (Fig. 3). Vertical velocities associated with these J.S. Stewart et al. / Deep-Sea Research II 95 (2013) 197–208 201

CCS-3 GOC-5 0 24 100 22 20

200 C) 18 ° 300 16 400 14

Depth (m) 500 12 10 600

8 Temperature ( 700 6 800 4 123456123456789 Day of Deployment

Fig. 3. Examples of Dosidicus gigas diving behavior for (A) CCS-3 and (B) GOC-5, with temperature overlaid on each point. Nighttime is shaded in gray. The oxygen minimum zone (OMZ: pink shaded area) and oxygen limited zone (OLZ: orange shaded area) are shown for the ﬁrst three days of tag deployments.

diel movements were quite low, with absolute values averaging OMZ. Squid in the GOC entered this region many more times than 0.0770.01 m/s for squid in the CCS and 0.0770.02 m/s in the did squid in the CCS, with 93 discrete events in the GOC compared GOC. Nighttime time-at-depth distributions were similar in both with 23 events in the CCS (Fig. 6A). The duration of most sojourns locations with overall median depths occupied by all tagged squid in the OMZ were o10 min (65.2% of all events in the CCS and in the two locations being 44.5 m (CCS) and 59.6 m (GOC) (Fig. 4A; 53.8% in the GOC), but much longer durations also occurred in Table 2). Daytime depths in CCS were generally deeper than those both locations. Descents lasting 42 h comprised 17.4% of the in GOC, but much overlap exists between the two distributions total excursions into the OMZ in CCS and 15.1% in the GOC. Events (Fig. 4B). Overall median daytime depths were 334.0 m (CCS) and with the longest durations within the OMZ lasted for 9.5, 7.0, and 255.7 m (GOC) (Table 2). Deep dives (41200 m) occurred during 6.5 h by squids GOC-6, GOC-4 and CCS-2, respectively. CCS-2’s four deployments (see Table 3 and Section 3.4), but these events did long event occurred during the ascent from a deep dive of 1387 m not greatly influence the overall depth distributions and are there- (Fig. 7: see Section 3.4); the other two long events in the GOC fore not illustrated in Fig. 4(A and B). Temperatures encountered occurred at the upper boundary of the OMZ and were not in the CCS both day and night are generally colder than GOC associated with deep dives. Squid also had more excursions into temperatures, with daytime temperatures in the two regions barely the OLZ in the GOC (n¼254) than in the CCS (n¼90) (Fig. 6B). The overlapping (Fig. 4C and D). Extremely cold temperatures (o5 1C) majority of these events were o1 h and never exceeded 5.5 h. in both locations are associated with deep dives (see Fig. 4 and Section 3.4). 3.3. Deep dives through the OMZ Distributions of nighttime temperatures in both regions had greater spread than the daytime distributions, particularly in the Four squid (CCS-1 and 4, GOC-3 and 4) made deep dives to GOC where surface mixed-layer temperatures can be extremely depths of 41200 m (Table 3), a level that approximates the lower high. In both locations, squid generally spent o10% of a 24-h boundary of the OMZ in both locations (Fig. 2; see also Roden, period at depths of r10 m, regardless of temperature (Fig. 5A). 1964). During these events squid passed completely through the However, they occasionally spent much larger amounts of time in OMZ into more oxygenated water below the lower boundary this zone when temperatures were 14–23 1C. Nearly all tagged (Fig. 7). Dives were initiated during both day and night. When squid spent a substantial amount of time at depths of r25 m in passing through the core of the OMZ, squid covered total vertical both locations (Fig. 5B), and in many cases for much greater distances of 500–1000 m at average speeds ranging from 0.07 amounts of time. to 0.80 m/s (Table 3), with respective transit times of 3.68–0.16 h. Time spent below the lower boundary of the OMZ ranged from 3.2. Interactions of squid with the OMZ and OLZ 2.46 h to 8.47 h, exposing squid to DO concentrations character- istic of the OLZ (20–60 mmol/kg; Fig. 7). CCS-4 was the only squid Median depth for the upper boundary of the OMZ in the CCS that made more than one deep dive, although the second dive did during the study period was 484.5 m, and the upper boundary of not exceed 1170 m. the OLZ was 256.9 m (Table 2). The upper boundaries of the OMZ and OLZ in the GOC showed overall medians of 209.7 m and 3.4. Jumbo squid diet 97.6 m, respectively. Thus, both the upper OMZ and OLZ are much shallower in the GOC than in the CCS. Although median daytime Results from diet analyses are reported from squid ranging in depth occupied by squid in the CCS (334.0 m) was deeper than size from 34 to 86 cm ML (mean 64.978.2 cm) in the CCS and 17 that in the GOC (255.7 m), the OMZ was also deeper in the CCS, to 85 cm ML (mean 48.7716.2 cm) in the GOC. In both areas and daytime DO concentrations experienced by squid were there- mesopelagic micronekton were the most frequently occurring fore higher in the latter region, with a median of 44.2 mmol/kg prey based on frequency of occurrence (%FO), with a rank order of versus 24.6 mmol/kg in the GOC (Table 2). Squid in the GOC also fish (primarily myctophids)4cephalopods4crustaceans4ptero- spent much more time within the OMZ (32.2% of total deploy- pods (Fig. 8A; Table 4). Consumption of coastal pelagic fishes, ment time) than did squid in the CCS (7.5%), but squid in both Pacific hake and various benthic fishes is considerably greater in locations spent 30% of the deployment within the OLZ (Fig. 4E the CCS, with hake and benthic fishes being only rarely encountered and F; Table 2). in D. gigas stomachs from the GOC. Most of the difference in Not only did squid in the GOC spend more time within the crustacean consumption between GOC and CCS is due to Pleur- OMZ, but there was also more diving activity at its upper oncodes planipes, an abundant micronektonic crab in the GOC that is boundary, resulting in more individual excursions into the upper generally absent from the waters sampled in the CCS. Cannibalism 202 J.S. Stewart et al. / Deep-Sea Research II 95 (2013) 197–208

CCS 20 GOC

10 Percent of Time 5

0 0 100 200 300 400 500 600 700 800 0 100 200 300 400 500 600 700 800 Depth (m)

Percent of Time 5

0 0 5 10 15 20 25 30 0 5 10 15 20 25 30 Temperature (°C)

20 18 16 14 12 10 8 6

Percent of Time 4 2

0 50 100 150 200 250 300 0 50 100 150 200 250 300 Dissolved oxygen (umol/kg)

Fig. 4. Nighttime and daytime vertical distributions for jumbo squid in the CCS (filled bars; n¼5) and the GOC (open bars; n¼6). Panels (A–D) display data from the entire deployments and panels (E, F) display data only from the first three days of deployments (see text). The dashed line indicates the upper boundary of the oxygen minimum zone (OMZ) at 20 mmol/kg dissolved oxygen and the dotted-dashed line indicates 60 mmol/kg dissolved oxygen. Nighttime panels are shaded. (A, B) Percent time-at-depth shown to 800 m (deep dives to 41200 had a negligible influence on the distribution), (C, D) percent time-at-temperature, (E, F) percent time-at-oxygen. Note that rapid deep dives through the OMZ followed by 2.5–8.5 h spent below the OMZ are reflected in these data, particularly in panel (D), where temperatures at depths 41200 m are much colder than normally encountered in the GOC.

Table 3 Deep dives by jumbo squid in the CCS and GOC. Average velocities are reported for periods of sustained swimming through the oxygen minimum layer (OMZ) for both descents (D) and ascents (A).

Tag number CCS-1 CCS-4a CCS-4b GOC-3 GOC-4 Time Night Dawn Day Dawn Night

DADADADADA

Distance of sustained swimming 956.2 868.6 465.9 498.2 597.5 593.1 900.0 840.9 798.0 802.7 Time of sustained swimming (h) 3.68 3.05 0.16 0.65 1.91 1.61 0.44 0.44 0.94 0.63 Average velocity of sustained swimming (m/s) 0.07 0.08 0.80 0.21 0.09 0.10 0.57 0.53 0.24 0.35 Maximum depth 1447.9 1387.7 1168.1 1397.3 1342.0 Time 41200 m (h) 2.46 8.47 – 2.75 3.8 appears to be substantially more frequent in GOC, but sampling Relative differences in the importance of these assemblages there was often within the area of the commercial squid fishery, are better clarified when prey are enumerated as the percent of which may bias such results. total number (%N) for fish and cephalopods only, because other J.S. Stewart et al. / Deep-Sea Research II 95 (2013) 197–208 203

60 CCS 50 GOC

10 Percent of 24−hour period

10 12 14 16 18 20 22 24 26 28 30 10 12 14 16 18 20 22 24 26 28 30 Mean temperature (°C)

Fig. 5. Percent of 24-h period Dosidicus gigas spent at two depth ranges: (A) depthsr10 m or (B) depthsr25 m, with associated temperatures. Error bars show 1 SD for temperature. More squid spent larger amounts of time at depthsr25 m.

50 150 CCS 50 20 GOC

40 15 30 10 20

Number of Events 5 10

0 100 200 300 400 500 600 700 0 50 100 150 200 250 300 350 Duration in the OMZ (minutes) Duration in the OLZ (minutes)

Fig. 6. Dosidicus gigas in low oxygen conditions: number of individual excursions into the OMZ and corresponding duration of these events in the CCS (open circles) and GOC (þsymbols). (A) Events within the OMZ (r20 mmol/kg DO) in the CCS (n¼23) and in the GOC (n¼93). (B) Events within the OLZ (20–60 mmol/kg DO) in the CCS (n¼90) and in the GOC (n¼254). Data are in 10-min bins. Note the breaks in the y-axes of both panels.

CCS-4 GOC-4 0 24 22 200 20 C)

400 18 ° 600 16 14 800

Depth (m) 12 1000 10

8 Temperature ( 1200 6 1400 4 1 2312 3 Day of Deployment

Fig. 7. Deep dives (41200 m) by Dosidicus gigas in autumn (A) CCS-4 and (B) GOC-4, with temperature overlaid on each point. Nighttime is shaded in gray. The oxygen minimum zone (OMZ: pink shaded area) and oxygen limited zone (OLZ: orange shaded area) are shown for the first three days of tag deployments. invertebrate prey are effectively impossible to enumerate reliably. include the larger fish prey discussed in conjunction with Fig. 8(A In this case, small mesopelagic fish represent 85% of all prey and B), namely coastal pelagics, Pacific hake, and benthic fishes. consumed in GOC, but only 46% in CCS (Fig. 8B). Cephalopods are approximately equally represented in both areas, at 15–20%. The remaining diet in CCS was again comprised of a much greater 4. Discussion percentage of coastal pelagic species, hake and benthic fishes, which together composed over 30% of the prey in the CCS, but Results in this paper indicate that jumbo squid are able to only 5% of those in the GOC. Based on %N, cannibalism accounts tolerate long periods of hypoxic conditions that are expected to be for only a small portion of the diet in both regions. physiologically stressful. Tagged squid spent about 30% of the In both locations D. gigas forages primarily on small prey that total time at liberty in the oxygen limited zone (OLZ, 20–60 mmol/ are 2–10 cm long, or 5–10% of the squid’s DML (Fig. 8C). kg DO) and up to another 30% in the oxygen minimum zone However, squid in CCS consume a greater proportion of larger (OMZr20 mmol/kg DO). Furthermore, they displayed rapid dives prey ranging from 15 to 40% of D. gigas DML, and these prey items and ascents completely across the core of the OMZ at average 204 J.S. Stewart et al. / Deep-Sea Research II 95 (2013) 197–208

micronekton 60 California Current Gulf of California 40

Frequency of 20 occurence (%)

0 fismeso cephalopods crustaceans pter coasfis hake fishbent D. gigas empty

opods tal pelagic hic h pelagic h

micronekton 80

40 Percent of 20 total number (%)

0 fismesopelag cephalopods coastalfis pelagic hake fishbenthic D. gigas

h h

Frequency (%) 20

0 0 5 10 15 20 25 30 35 40 45 50 Prey length relative to predator length (% DML)

Fig. 8. Diet composition of Dosidicus gigas. (A) The percent frequency of occurrence, (B) percent of total number (%N) of fish and cephalopod prey only, and (C) the relative size (as percentage of predator dorsal mantle length) of prey items for which length could be estimated. speeds of up to 0.8 m/s. Hypoxic depths may provide jumbo squid the OMZs are quite different. First, how is jumbo squid vertical with a refuge or escape route from predators, but they are also distribution influenced by the OMZ in the two study areas? likely to provide a distinct foraging advantage. Jumbo squid Second, how does foraging behavior differ between the two primarily feed on small mesopelagic fishes and cephalopods, locations? Third, what benefits might be provided by the see- animals that are typically part of the acoustic deep scattering mingly hostile environment of the OMZ? Fourth, how might long- layer (DSL). These organisms often spend daytime at depths just term shoaling of midwater hypoxic environments impact jumbo above the OMZ (Koslow et al., 2011), where physiological con- squid and contribute to its range expansion? straints associated with hypoxia may prevent them from going deeper. The ability of jumbo squid to occupy the upper OMZ and 4.1. Jumbo squid vertical habitat and hypoxia OLZ and to forage there could give them an advantage over other competing aerobic predators with which squid may compete. Jumbo squid were exposed to hypoxic conditions (20–60 mmol/kg In this study we address several questions concerning the DO in the OLZ and r20 mmol/kg DO in the OMZ) for the vast association between jumbo squid and midwater hypoxic regions majority of the daytime (Fig. 4F)anduptohalfofthetotaltimeat by comparing two environments where the upper boundaries of liberty (total fraction of time in OLZ and OMZ: Table 2). Although J.S. Stewart et al. / Deep-Sea Research II 95 (2013) 197–208 205

Table 4 Trophic groups used in diet analyses and Fig. 8, with important families for both regions as well as species separately for the CCS and the GOC.

Trophic group Important families Gulf of California California Current

Mesopelagic Myctophidae, Bathylagidae, Paralepididae Benthosema panamense, Triphoturus mexicanus, Tarletonbeania crenularis, Stenobrachius fishes Diogenichthys laternatus leucopsarus, Diaphus theta Cephalopods Gonatidae, Pyroteuthisdae, Pterygioteuthis giardia, Abraliopsis affinis, Gonatus Gonatus onyx, Onychoteuthis borealijaponicus, Enoploteuthidae, Loliginidae Doryteuthis opalescens Coastal pelagic Engraulidae, Clupeidae, Osmeridae Engraulis mordax, Sardinops sagax Engraulis mordax, Sardinops sagax, Clupea pallasi, fishes Allosmerus elongatus Pacific hake Merluccidae Merluccius angustimanus Merluccius productus Benthic fishes Scorpaenidae, Cottidae, Pleuronectidae, Porichthys sp., Physiculus spp. Sebastes jordani, Psychrolutes paradoxus, Moridae Glyptocephalus zachirus Crustaceans Galatheidae Euphausidae, Seregestidae, Pleuroncodes planipes, Euphausidae, Plesionika sp. Euphausidae Seregestes sp., unidentified decapods Pandalidae Pteropods Cavoliniidae, Limacinidae Cavolinia sp., Clio sp., Limacina sp. Clio pyramidata, Caranaria japonica, Cresis spp. the depths of the OLZ and OMZ in the CCS were substantially of caloric input conferred by these latter three fish groups to total deeper than in the GOC (Table 2), we do not believe that this consumption and energy throughput in CCS vs. GOC is likely to be physical factor is directly responsible for the deeper daytime depth even greater, because the average size and mass of these prey distribution of the squid in the CCS. This subject is discussed in items is generally much larger than the size of mesopelagics (see detail in Section 4.2. Field et al., 2013). Nighttime depth distributions in both locations were similar, In the GOC, there is no significant relationship between the with squid occupying primarily the upper 100 m of the water size of jumbo squid and the size of prey consumed (Markaida and column (Fig. 4A). Regardless of the surface temperature in the CCS Sosa-Nishizaki, 2003; Markaida et al., 2008), because squid or GOC, squid generally spent o10% of each day in the top 10 m, primarily consume mesopelagic micronekton. This is similar to but up to 60% of a given day was spent in the upper 25 m. Most of the pattern in the CCS, but in this case there is a tendency that the these shallow excursions occurred during nighttime, and we larger fishes (primarily Pacific hake but also benthic groundfish assume that a long occupancy of this zone was associated with 425 cm total length) are consumed by larger squid (Field et al., opportunistic foraging on small pelagic fishes. Squid in the GOC 2007, 2013) such as those involved in the tagging study. This rarely entered the upper 10 m when temperature exceeded 23 1C, difference might be attributed to the fact that hake (or an consistent with the hypothesis that such high temperatures inflict ecological equivalent) do not reach comparable levels of abun- physiological stress (Davis et al., 2007; Rosa and Seibel, 2010). dance (or size) in the GOC, so this resource would appear to be Four of eleven tagged squid (36%) carried out single dives of less available there. 41200 m during the deployment period, with one squid (CCS-4) A greater reliance on larger, coastal pelagic and benthic prey in making a second dive of 41000 m during its three-day deploy- the CCS should also be viewed in terms of the time spent at ment. Deep dives were initiated during both daytime and night- depths of o60 m at night in this region (Fig. 4A). This increased time, in most cases from depths of o75 m, well above the OLZ. In occupancy of shallow nighttime depths probably represents more each case the squid swam actively through the entire OMZ time spent foraging for these organisms on the larger shelf without pausing. Sustained vertical velocities involved in crossing environment in the CCS (relative to GOC), and this would tend the OMZ varied substantially and ranged up to 0.8 m/s (Table 3). to enrich the diet with larger fishes. Pacific hake in the CCS are Vertical velocities associated with crossing the OMZ were higher typically found at the edge of the shelf in large schools (Holmes than those recorded after the squid crossed the lower boundary et al., 2008), and horizontal migrations of squid onto the shelf at into a region with DO concentration similar to that in the OLZ. nighttime (Stewart et al., 2013) would involve travel through this This conclusion is evident by inspection of the records in Fig. 7 habitat in certain areas. Thus, a paucity of larger forage fishes in and is also born out by comparisons of vertical velocity distribu- the GOC in conjunction with a greatly reduced shelf environment tions associated with these deep dives in the two regions, which and seasonally very warm temperatures at shallow depths would identified 3.2 m/s as the highest velocity when GOC-4 descended all act to limit the amount of large coastal fishes consumed by through the OMZ (data not illustrated). These active dives large squid in the GOC. through the extremely hypoxic core of the OMZ may represent an anaerobic performance limit. Squid remained at depths of 4.3. Benefits of OMZ occupancy 41200 m for several hours before ascending through the OMZ, again without pausing, and tended to slow down once they Hypoxia is a consistent environmental feature associated with reached the OLZ. The frequency at which these deep dives were the daytime vertical distributions of squid in both locations. The observed strongly suggests that this behavior is not uncommon. ability of ‘‘jumbo’’ squid of all sizes (juveniles to adults) to operate for hours in such low oxygen conditions is due in part to highly 4.2. Diet and foraging behavior effective regulation of oxygen consumption that reduces metabolic rates (Gilly et al., 2006; Rosa and Seibel, 2008), and it has Small mesopelagic fish and cephalopods dominate the diet in been suggested that these physiological effects would limit adult both regions in terms of frequency of occurrence (Fig. 8A) and activity and feeding at hypoxic depths (Rosa and Seibel, 2010). total number of prey items (Fig. 8B). These two groups account for Significant reduction in swimming activity (as defined by vertical 65% of the total number of dietary items that could be reliably velocity distributions) has recently been reported from PAT tag enumerated in the CCS and 96% in the GOC. The remainder of diet data for large squid in the GOC, with vertical velocities in the OMZ composition shows a striking regional difference. Coastal pelagics, being reduced by 50% or more relative to the OLZ or the upper hake, and benthic fishes account for nearly all of the rest of the 100 m of the water column (Gilly et al., in press). diet in the CCS, whereas these groups are virtually non-existent in Despite reduced metabolic rates and activity levels, foraging stomach samples from GOC. Regional disparity in the proportion by jumbo squid under OMZ conditions may still be possible. 206 J.S. Stewart et al. / Deep-Sea Research II 95 (2013) 197–208

Foraging under OMZ conditions has been observed from remotely Vetter et al., 2008, respectively). In contrast, D. gigas can remain in operated vehicles (Rosa and Seibel, 2010), and seemingly little this environment for many hours. effort is required to capture prey (Zeidberg and Robison, 2007). Individual excursions into the upper OMZ could also relate to The diel vertical migrations of jumbo squid would allow access to avoidance of visual predators, and our data in both locations, its main source of prey (mesopelagic micronekton) both day and particularly in regard to the longer forays within the upper OMZ, night. These prey items would probably tend to be somewhat are consistent with this idea. However, taking refuge in this lethargic at cold, hypoxic, daytime depths, so active hunting limited region would perhaps not be very effective at avoiding might be possible at quite low speeds. Thus, we propose that breath-holding mammals (Davis et al., 2007), and thus the inhabiting a hypoxic environment during the daytime provides energetically costly and physiologically stressful deep dives jumbo squid with two main advantages: to forage with minimal reported in this study may represent avoidance or escape effort and to avoid predators in a hostile environment. This would responses to mammalian predators. The amount of time involved be true of both the GOC and CCS. in these deep dives—particularly because squid remain below the In some areas the daytime depth distribution of many meso- OMZ for several hours—would exceed the capabilities of any pelagic organisms can be limited by the OMZ, which acts as a marine mammal, as the average deep dive of a sperm whale lasts hypoxic barrier that concentrates micronekton into a well- 40–50 min (Davis et al., 2007; Watwood et al., 2006). A squid defined DSL (Koslow et al., 2011). Unfortunately, daytime depths need only dive below the OMZ and either wait there or migrate of the DSL in the two regions where squid tagging was carried out horizontally before ascending in order to escape. are not extensively documented, but typical values would be Fig. 9 shows representative depth ranges and greatest reported 250–350 m in the Guaymas Basin (WFG and K. Benoit-Bird, depths for the major known predators of adult jumbo squid. Four unpublished data) and 350–500 m in the southern CCS (Koslow of these predators are capable of dives to 41000 m through the et al., 2011). In both regions these values are similar to median OMZ in the regions where we tagged squid—sperm whales, daytime depth of jumbo squid (256 m in the GOC vs. 334 m in the northern elephant seals, and bigeye and yellowfin tuna. Several CCS). The important difference is that in the CCS the upper others (hammerhead shark, swordfish and bluefin tuna) can reach boundary of the daytime DSL appears to be 150 m shallower 1000 m, and escape from these predators might also induce than that of the OMZ, whereas in the GOC the two boundaries are jumbo squid to make a deep dive. In the Guaymas Basin of the similar. GOC, sperm whales would probably be the only realistic candi- Hunting DSL organisms from within the OLZ and OMZ could dates, as they are in high abundance in this area and are known to give jumbo squid a distinct advantage over competing aerobic eat large adult jumbo squid (Davis et al., 2007). Off the coast of predators. A number of large pelagic fish, particularly tunas, central California in the CCS, sperm whales, elephant seals, and swordfish and mako sharks, make putative foraging dives to the swordfish are likely to be capable of consuming a full-sized jumbo depth of the upper OMZ, but they are limited by both low oxygen squid and abundant enough to merit consideration. Squid smaller and low temperature (Dewar et al., 2011; Schaefer et al., 2011; than those tagged here would be subject to predation by any of

Cetaceans PinnepedsElasmobranchs Teleosts Mako shark* Blue shark Striped marlin Bigeye tuna White shark* Yellowfin tuna Humboldt squid Pilot whale Swordfish* Bluefin tuna California sea lion Hammerhead shark Risso’s dolphin Sperm whale* Northern elephant seal* Bigeye thresher shark 500 Common thresher shark Depth (m)

1000

1500 1900 m

Fig. 9. General depth ranges of Dosidicus gigas and some of its frequent predators, assembled from the literature. Solid bars show representative depth ranges and dotted lines show the maximum depth observed through electronic tagging. Asterisks indicate predators capable of feeding on large adult D. gigas as in the present study (50– 80 cm ML). References are as follows: sperm whales (Physeter macrocephalus)(Davis et al., 2007); pilot whales (Globicephala melas)(Sakai et al., 2011); northern elephant seals (Mirounga angustirostris)(DeLong and Stewart, 1991; Le Boeuf et al., 2000); California sea lions (Zalophus californianus)(Costa et al., 2007); Risso’s dolphins (Grampus griseus)(Wells et al., 2009); mako sharks (Isurus oxyrinchus)(Vetter et al., 2008; Musyl et al., 2011); hammerhead sharks (Sphyrna lewini) (Jorgensen et al., 2009); bigeye thresher sharks (Alopia superciliosus)(Weng and Block, 2004); common thresher sharks (Alopias vulpinus) (Cartamil et al., 2010); white sharks (Carcharodon carcharias)(Boustany et al., 2002); blue sharks (Prionace glauca)(Weng et al., 2005; Musyl et al., 2011); swordfish (Xiphias gladius)(Carey and Robison, 1981; Dewar et al., 2011); bluefin tuna (Thunnus thynnus)(Teo et al., 2006); bigeye tuna (Thunnus obesus)(Schaefer and Fuller, 2010); yellowfin tuna (Thunnus albacares) (Schaefer et al., 2007, 2011); striped marlin (Tetrapturus audax)(Sippel et al., 2007). J.S. Stewart et al. / Deep-Sea Research II 95 (2013) 197–208 207 the deep-diving predators in Fig. 9, but we have no information Paull, C. Huffard, W. Matsubu, J. O’Sullivan, L. Anglin, D. Minard, H. on diving behavior of smaller squid. Bruning and E. Larson and in the GOC: C. Salinas and his students, particularly J. Ramos. S. Haddock provided access to MBARI 4.4. The shoaling of the OMZ and jumbo squid range expansion oceanographic profiles from the internal database, and A. Swee- ney supplied the deep CTD-O data from the R/V New Horizon During the last several decades the upper boundary of the (support from Office of Naval Research N00014-09-1-1053). K. OMZ has been shoaling in the CCS (Bograd et al., 2008; McClatchie Benoit-Bird, D. Staaf, L. Zeidberg, A. Booth, P. Daniel and two et al., 2010), and this trend is predicted to continue (Keeling et al., anonymous reviewers provided valuable comments about the 2010; Rykaczewski and Dunne, 2010). Our study compares the manuscript. We also give special thanks to J. Hamlin and J. Pungor behavior of D. gigas in relation to the OMZ in the CCS to an who recovered tag CCS-6 in Maui. Work in the CCS was supported environment in the GOC where the OMZ is much shallower. This by Grants from California Sea Grant and California Ocean Protec- comparison can provide insight as to how the vertical habitat tion Council (R/OPCFISH-06); work in the GOC was supported by utilization and foraging activities of this large predator might the National Science Foundation (OCE0526640 and OCE0850839) change in response to long-term physical changes in the mid- and the David and Lucile Packard Foundation. This paper is a water environment in the CCS. contribution to a CLIOTOP initiative to develop understanding of Daytime depth of the DSL often converges on the upper squid in pelagic ecosystems. boundary of the OMZ when it is shallow, so much so that in the Humboldt Current off Peru acoustic surveys can accurately indicate the depth of the OMZ (Bertrand et al., 2010). As the References OMZ shoals, the midwater habitat of migratory DSL organisms may be vertically compressed as their daytime zone of occupancy Bazzino, G., Gilly, W.F., Markaida, U., Salinas-Zavala, C.A., Ramos-Castillejos, J., is pushed towards the surface (Koslow et al., 2011). The eastern 2010. Horizontal movements, vertical-habitat utilization and diet of the jumbo squid (Dosidicus gigas) in the Pacific Ocean off Baja California Sur, Mexico. Pacific contains the world’s largest and most shallow OMZ, so Prog. Oceanogr. 86, 59–71, http://dx.doi.org/10.1016/j.pocean.2010.04.017. even relatively small amounts of shoaling or intensification could Bertrand, A., Ballo´ n, M., Chaigneau, A., 2010. Acoustic observation of living greatly augment habitat compression (Keeling et al., 2010). A organisms reveals the upper limit of the oxygen minimum zone. PLoS One 5, e10330, http://dx.doi.org/10.1371/journal.pone.0010330.t002. recent hypothesis to explain the decreased abundance of larval Bograd, S.J., Castro, C.G., Di Lorenzo, E., Palacios, D.M., Bailey, H., Gilly, W.F., mesopelagic fishes in the southern California Bight is that this Chavez, F.P., 2008. Oxygen declines and the shoaling of the hypoxic boundary habitat compression brings DSL organisms to depths during in the California Current. Geophys. Res. Lett. 35, 6, http://dx.doi.org/10.1029/ 2008GL034185. daytime that are more illuminated, thereby increasing suscept- Bograd, S.J., Sydeman, W., Barlow, J., Booth, A., Brodeur, R., et al., 2010. 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