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Notice: ©2009 Inter-Research Science Center. This manuscript is available at http://www.int-res.com/ and may be cited as: Jacoby, C. A., Youngbluth, M. J., Frost, J. R., Flood, P. R., Uiblein, F., Båmstedt, U., Pagès, F., & Shale, D. (2009). Vertical distribution, behavior, chemical composition and metabolism of Stauroteuthis syrtensis (Octopoda:Cirrata) in the Northwest Atlantic. Aquatic Biology, 5(1), 13-22. doi:10.3354/ab00117. _- - Vol. 5: 13-22, 2009 AQUATIC BIOLOGY Printed March 2009 Published online Pebrusrv s. 2009 doi: 10.3354/ab00117 Aquat BioI 1

Vertical distribution, behavior, chemical composition and metabolism of Stauroteuthis svrtensis (Octopoda: Cirrata) in the northwest Atlantic

3 Charles A. Jacoby':", Marsh J. Younqbluth", Jessica R. Prost':", Per R. Flood , 4 Franz Uiblein , Ulf Bamstedt", Francese Paqes'':", David Shale?

'University of Florida, Gainesville, Florida 32653, USA '!IIMhor Branch Oceanoqraphlc InsliLution at Florida Atlantic University, 5600 Highway 1 North, Fort Pierce, Florida 34946, USA "Bathybtoloqica A/S, Gerhard Grans vei 58, 5081 Bergen, Norway "Institute of Marine Research, Nordnesgaten 33, PB 1870 Nordnes, 5817 Bergen, Norway sUmeiI Marine Sciences Centre, Norrbyn, 910 20 Hornetors, Sweden "Institut de Ciencies del Mar (CSIC), Passeig Marilim de Ia Barceloneta 37-49,08003 Barcelona, Spain 714 Victoria Avenue, Swanage, Dorset BH19 IAN, UK "Present address: Institute for Hydrohiology and Fisheries Science, University of Hamburg, Olbersweg 24, 22767 Hamburg, Germany

ABSTRACT: The cirrate octopod Stauroteuthis syrtensis is a mesopelagic species commonly collected in the North Atlantic. Individuals were observed at depths >600 m and typically within 100 m of the bot­ tom in three -900 m deep canyons indenting the southern edge of Georges Bank. When first sighted, most octopods were floating passively with their webbed arms gathered into a small ball. When dis­ turbed, they expanded their webs to form a 'balloon' shape, swam slowly by sculling their fins, pulsed their webs like medusae and, in some cases, streamlined their arms and webs and moved away smoothly by rapidly sculling their fins. The bodies of 9 octopods comprised 92 to 95 '}';, water, with tissue containing 9 to 22 'X, carbon (C) and 2 to 4 % nitrogen (N). These values were similar to those reported 1 for medusae and ctenophores. Oxygen (02) consumption rates of 4.6 to 25.8 umol O 2 rr C h- were within ranges reported for medusae, ctenophores, and deep-water cephalopods. The stomachs of S. syrtensis, dissected immediately after capture, contained only the calanoid copepod Calanus tinmarchi­ cus. Calculations indicated that S. syrtensis need 1.3 to 30.1 indo d- 1 of C. titunatcbicus to meet their ~lg measured metabolic demand. Excretion rates (0.3 to 12.4 NH4+ s' C h' and Cl.06 to 4.83 pg 1'04]­ U C· II !) we'll; dt ledsL <111 order of muqnitudo lower th.in Idtes reported for other octopods or gelatinous zooplankters. O:N ratios (11 to 3(6) suggested that S. svrietisis catabolized lipids, which may be sup­ plied by C. Iinnuucbicus. Vertical distribution, relatively torpid behavior and low metabolic rates char­ actcrizcd S. svrtetisis as d benthopelaqic and relatively passive predator on copepods.

KEY WORDS: Stauroieuthis svrtensis . Respiration . Excretion ' Chemical composition . Vertical distribution' Behavior

------Resnlc or republication not permitted without written consent of the publisher ----"""------

INTRODUCTION mens caught in bottom trawls and higher abundances reported at depths of 1500 to 2500 ill (e.g. Collins & Stauioteuthis syrtensis Verrill, 1879 is a deep-water Henriques 2000, Collins et aL 2001, 2002, Vecchione & octopod that occurs throughout the North Atlantic Galbraith 2001, Vecchione & Pohle 2(02). Specimens (Collins & Henriques 2000, Collins et ell. 2002, Collins captured at depths of 250 to 500 rn off Greenland and & Villanueva 20(6). Most specimens have been col­ Iceland provided evidence that the vertical distribution lected at depths of 500 to 4000 In, with many speci- of this species was influenced by water temperature as

• Email: [email protected] © Inter-Research 2009' www.int-res.corn t Decedsf~d 14 Aquat BioI 5: 13- 22, 2009

Iceland provided evidence th at the vertical distribution of th is species was influenced by water temperature as much as, or more so th an, depth (Collins 2002) . Stsutote utbis syrtensis ha s been observed to display a variety of behaviors, including swimming by sculling its paired fins , swimmi ng via medusoid contractions of its web complex , inflating its web to varying degrees, and inve rting its arms and web to expose suckers that differ from those of most octopods in that they contain bioluminescent photophores and ar e not adhesive (Vecchione & Young 1997, Johnsen et al. 1999, Collins et al. 2002, Collins & Villanueva 2006) . Inflation and inv ersion of the web have been hypothesized to be defensive responses to disturbance or behaviors involved in capturing small cru stacean pr ey attracted by the biol uminescence emanating from the sucke rs (Vecchione & Young 1997, Johnsen et al. 1999, Collins et al. 2002). A se condary web that links the arms to the primary web in S. syrtensis and other Cirr ote uthidae facilitat es behaviors su ch as medusoid swimming, inflation and inv ersion. Sim ilar to other members of the suborder Cirra ta, Stauroteuthis syrtensis possesses a fragile, se mi-gela ti­ Fig . 1. Locat ion s of sampling for cirra te oc topods Stauro­ nous body (Collins & Henriques 2000 , Collins et al. teutbis syrten sis 2002), which suggests that th e met abolic rat es of S. syrtensis should resemble those of medusae and cteno­ in Oceanographer Canyon during September 2004 . At phores, rather than the higher respiratory demands of the sampling stations, dates, times, depths, tempera­ more mu scular cepha lopods . In addition, if S. syrten sis tures, sali nities, and conce ntrations of dissolved O2 am bushes pr ey, perhaps by using its bioluminescent wer e recorded with Seabird SBE 25 Sealoggers. suc ke rs as lur es, th en its O 2 consumption rates should Octopods and water samples without visible organ­ be relatively low and similar to other deep-water isms (i.e. controls) were collected in 6.5 I acrylic sam­ ce phalopods that have replaced visually guided pur­ plers that had been washed with a 1 mol l"! HCI solu­ suit of pr ey with an ambush strategy (Childress & tion prior to use (Tietze & Clark 1986) . An individual Mickel 1985, Seibel et al. 2000, Seibel & Carlini 2001). sampler contained either 1 individual of Stauroteuthis The present study provides the first measurements of syrtensis or a control water sample. 3 O 2 consumption and NH 4+ and P04 - excretion for Measu rements of respiration an d excretion. Upon Stauroteuthis syrtensis collected in Oceanographer return to the surface, samplers were transferred Ca nyon, a deep-water canyon that indents the south­ quickly from the submersible to a dark room main­ ern bo unda ry of Ge orges Bank. Furthermore, in situ tained at an air temperature of 4 to 5°C, which mim­ observa tions from cre wed subme rsibles documented icked in situ conditions. Within 28 h of capture, all the vertical distribution and behavior of these octopods octopods excep t the largest individual (wet weight, in this and 2 adj acent canyons, Hydrographer and WW = 158 g) were transferred gently into 0.5 to 2.2 I Lydonia Canyons. ac rylic chambers. Th es e smaller chambers, which acted as respirometers, were filled and sealed in a manner that avoided the formation or trapping of air MATERIALS AND METHODS bubb les . When additional water was needed to fill a sma lle r chamber, seawater collecte d in Niskin bottles Observation and collection. Stauroteuthis syrtensis from 800 to 900 m water depth was added. Th e largest were observed from 'J ohnso n-Sea-Link' submersibles, individual was too large for th e smaller chambers, so it which operat e to a depth of 914 m (Youngbluth 1984). was incubated in the original 6.5 I sampler, which Visual obse rva tions were made in Hydrographer, se rved as a respirometer. Oceanographer and Lyd on ia Canyo ns during June An experiment consisted of on e or more respirome­ 1995, September 2001 , June 2002 , September 2003, ters, each holding a single octopod, and a respirometer September 2004, and October 2005 (Fig . 1). Individuals that contained water without visible organisms, which for studies of respiration and excre tion wer e collected yielded measures of background changes in concen- Jacoby el al.: Distribution, behavior and metabolism of Steuroteuthis syrtensis 15

trations of dissolved 02, NH4 + and 1'04 :1- . Antibiotics to the nearest 0.1 g over a period of 2 to 4 d. Each dried were not added to any of the rcspirometors. During specimen was thoroughly homogenized, and aliquots experiments, all respiromctcrs were kept in darkness were sent to the Analytical Laboratory of the Marine at 4 to 5°C and ambient pressure (1 atm) for 9 to 22 h. Science Institute at the University of California, Santa (}, consumption WdS mou surod concurrently in con­ Barbara, where proportions of C, Hand N were deter­ trol and experimental respirometers with a noninva­ mined using a Perkin-Elmer Model 240 elemental ana­ sive, rnicro-optode system (PreSens. http://microoptode. lyzer and an acetanilide standard. com/html/stert.htrnl). O 2 concentrations (prnol O 2 1 J) were loqqcd at 1 s intervals. In some experiments, re­

I (II dlllJl S \V( 'II' cond uctocl tor :30 min periods, separated RESULTS by :30 to 60 min intervals, so that O 2 consumption could be trucked in multiple respirometers using a single Vertical distribution micro-optode system. Records from the initial 2 to 6 h were excluded from estimates of O 2 consumption to Eighty-one Steuioteutbis syrtetisis were sighted in 4 eliminate periods of equilibration and acclimation. canyons during 24 dives conducted during 6 cruises.

Rates of O 2 consumption were calculated using least­ Approximately 90 %, of the octopods were recorded as squares linear regression, and only the results of statis­ single individuals in a field of view that encompassed tically significant regressions were used. If controls approximately 400 m' of water. The maximum number yielded statistically significant rates of O 2 consumption, of individuals sighted in a single field of view was 5; these values were subtracted from the appropriate ex­ this observation took place at approximately 14:00 h on pori mt-nla! rdtes to account for respiration by organisms 7 September 2002 at a depth of 848 m in a water other than Stnutoteuttiis syrtensis. column of 1000 rn in Oceanographer Canyon. Winkler titrations were performed on duplicate water Steuroteutliis syitensis were sighted at depths of 60:3 samples removed from representative respirorneters to 908 m (mean ± SE: 780.9 ± 8.:3 m: Table 1). The oc­ (Wetzel & Likens 20(0). When compared to records topods were observed from -0.5 to 258 m above the from micro-optodes, these measurements provided a bottom (100.1 ± 7.2 rn]. The 35 individuals observed check on the reliability of the time series. during daytime dives (14:00 to 17:00 h) and the 46 in­

Duplicate samples for estimating NH 4+ excretion and dividuals observed during nighttime dives (20:00 to \'itlH:J duplicdte: OJ smgll' sum ph-s lor cstim.rtinr; PO'/ 00:30 h) were sighted at similar, but significantly differ­ excretion were extracted from an acrylic sampler at the ent distances above the bottom (daytime 81.2 ± 10.6 m, beginning of en experiment, i.e. an initial control, and nighttime 114.4 ± 9.2 m, t = -2.:37, df = 7:3, P < 0.05). from control and experimental respirorneters at the Octopods were collected or sighted in water with tem­ end of the incubation periods. Due to a contaminated peratures ranging from 4.20 to 6.14°C (4.67 ± 0.06°C), filtc'rinu apparatus and unavoidable delays in obtain­ salinities ranging from :34.86 to :35.03 psu (:34.96 ± ing a replacement bulb for the spectrophotometer, 0.01 psu). and dissolved O 2 concentrations ranging these samples were not filtered, and they were frozen from :3.00 to 5.54 mll-J (4.83 ± 0.16 ml l") (Table 1). at -20°C for up to 11 d before analysis. Concentrations were determined by standard spectrophotometric methods using a Spectronic Genesys 8 spectrophoto­ Behavior meter, with a 10 cm cuvette at 640 nm for NH.j' and 3 882 nm for 1'°4 - (Strickland & Parsons 1972, American When first sighted, most Steutoteutbie syrtensis Public Health Association 1989). Rates of NH/ and were floating passively, with their arms contracted, POll excretion not attribut.able to Stauroteuthis svr­ webs curled into a small ball and eyes hooded. When teusis were calculated using concentrations in the disturbed, seemingly by light, noise, or turbulence appropriate initial and final controls, and these values from the submersible, octopods would expose their were subtracted from rates calculated using final con­ eyes and unfold their webs, which they often inflated. centrations in experimental rospirometers and initial Initially, octopods tended to move away from the sub­ concentrations from the appropriate controls. Only mersible by scullinq their fins or pulsing their webs positive differences were reported. like a medusa. Eventually, some octopods streamlined Following experiments, Stauroteuthis syrtensis were their webbed arms behind their bodies and increased transferred to tared pans and frozen (-20°C). In a the rate at which their fins sculled to move away from shore-based laboratory, each frozen specimen was the submersible smoothly and more rapidly. ihuwcd und us WW wus recorded to the ncurost 0.1 D. Neither hunting nor feeding behavior was observed, After determination of WW, specimens were dried at which was expected given the response of the octo­ I)OOC unlil d conslstcnt dry weight (DW) was obtained pods to disturbance from the submersibles. The guts of Hi Aquat BioI 5: 13-22, 2009

Tabl« 1 Sli/uroteuthis svrtonsi«. Details for collections and siqhtinqs of cirrate octopods from Ocoanoqrapher Canyon for use in metabolic experiments. Salinity was consislantly 35 psu. -: data nol applicable

Octopod Date Latitude, Longitude Time of Depth of Depth oj Temperature Dissolved

collection collection bottom (0C) O2 (h) or sighting (m) (mill) (m) ...... __....._--_..--..------...... _-_._- ...... _._--_.._-_.. 17 Sep 2004 40020.1B2N,6eoOB.277W 14:45 BBB 930 4.30 5.52 2 B07 4.37 5.4B 3 40° 20.427 N, fiB"OB.291 W 22:42 784 910 4.60 5.35 ""')C 22:53 f ",.,,) 4BO 5.25 .5 21:4<3 821 4.59 5.36 I' 21:25 90B 4.44 5.42

7 22 Sep 2004 40° 19.996 N, 6sa 07.997 W 14:45 741 913 4.74 5.28

B 40° 20363 N, 6sa 08.250 W 21:35 857 910 4.86 5.21

9 23 Sep 2004 40° 20.057 N, 6no 07.890 W 21:38 861 912 4.67 5.30

All collections & siqhlinqs 780.9 881.0 4.66 4.829 (mean ± SE) ± 8.3 ± 6.4 ± 0.063 ± 0.155

3 individuals captured during 3 different dives were WW = 0.98, elf = 8, P > 0.10; DW = 0.98, elf = 8, P > 0.10; dissected imruediutelv after completion of the dives. anel C content =0.98, df = 8, P > 0.10; Cochran's tests for The stomachs contained 8 to 25 intact or partially DW versus WW =0.54, elf = 2,8, P > (l.05; C content ver­ digested Calanus finmarchicus. The calanoids exhib­ sus WW = 0.24, elf = 2,8, P > 0.05; and C content versus ited no evidence of dismemberment, and they were DW = 0.60, df = 2,8, P > 0.(5). Statistically significant mostly Staqe V copepodites along with a few adults. linear regressions that explained> 80 'Yo of the variation These crustaceans were never observed in water sam­ in the data revealed that all 3 measures of size were pies used as controls in metabolic experiments, so it related and reliable (Fig. 2). WdS unlikely that the octopoels fed after capture. C. fin­ Duplicate Winkler titrations from 8 of the 9 experi­ nuuchicus occurred in all of the canyons and, in 2002, ments had coefficients of variation < 5 (1<,. These data a series of 26 samples taken at depths of 430 to 750 rn were homoscedastic and normally distributed (Coch­ wil h d suction sdmplel' mounted on the submersible ran's test = 0.55, df = 2,7, P > 0.05; Ryan-Joiner tests for I violdod el mran abundance (±SE) of 31.2 ± 3.4 indo m-: Winkler values = 0.94, df = 7, P > 0.10; and micro­ across the :3 canyons. optode values = 0.92, df = 7, p » 0.(5). A statistically siqnificant linear regression indicated that measure-

Chemical composition, O 2 Table 2. Stnuroieutbi« syrtensis. Weighls and elemental composition of cirrate consumption, and excretion octopods. OW: dry weight

Nine Stnuroteuihis syrtensis were Octopod WeiCJht(CJ) Proportion Proportion of OW C content used in experiments (Table 1). All octo­ Wet Dry of water C HN (9) pods were captured within 185 m of the - ...... _....- ...... _.._------...... _....__.- ..-.-.-.~-- .._- ...... _--_..--_..------...... _.._..- sea floor in a water column of 910 to 1 74.2 3.5 0.95 0.198 0.033 0.032 0.69 930 m. WW and DW of those octo­ 2 13.2 1.1 0.92 0.144 0.026 0.024 0.16 147.7 6.8 0.95 0.174 0.029 0.031 1.18 pods varied by an order of magnitude 3 4 21.9 1.0 0.95 0.091 0.020 0.018 0.09 (Table 2). Water comprised 92 to 96'1:, 5 38.8 1.7 0.96 0.108 0.021 0.024 O.lB of the entire bodies of all octopods 6 13.2 0.7 0.95 0.156 0.026 0.021 o.i i (Table 2). C:N ratios ranged from 4.57 to 7 21.9 1.8 0.92 0.181 0.030 (UJ28 0.33 8 50.2 2.7 0.95 0.107 0.020 0.022 0.29 7.60, with a mean (±SE) of 5.77 ± 0.31. 9 158.1 9.6 0.94 0.224 0.039 0.042 216 WW, DW and C contents were normally Mean 59.91 3.21 0.943 0.1537 0.0271 0.0269 0.577 distributed and homoscedastic after loglll ± SE ±18.76 ± 1.01 ±O.005 ±0.0151 ±0.0021 ±0.O024 ±0.230 transformation (Ryan-Joiner tests for .lacoby et al.: Distribution, behavior and metabolism of Siauroteuthis svrtensis 17

1.5 merits. Weight-specific and C-specific rates of O con­ L0910(DW) =-1.1 + 0.9 x L0910(WW) a 2 sumption varied among octopods, with ranges of 0.031 R2 = 0.93, P < 0.001 1.0 to 0.243 umol O 2 g-l WW h", 0.576 to 3.192 urnol O 2 9 • 1 s' DW n:'. and 4.631 to 25.788 pmol O 2 s' C h- S (Table 3). With the values for Octopod 9 excluded, ~ 0.5 0 weiqht-spccific and C-specific rates of O 2 consumption OJ 0 • decreased as body size increased, with the models fit -.J • 0.0 • • to WW and C content explaininq a larger amount of • variation in the data (Fig. 3). Octopod 9 was the largest -0.5 individual and, although there was no evidence of 0.0 0.5 1.0 1.5 2.0 2.5 unusual behavior, this individual may have had em Log1Q[WW (g)] imperceptible injury resulting in stress and greater O 2 consumption. As expected, data standardized to DW 1.5 varied more than data standardized to C content due to L091O(C) =-2.2 + 1.0 x L091O(WW) b the difficulty of removing bound Welter from gelatinous 1.0 R2 = 0.82, P =0.001 tissue (Youngbluth et al. 1988). 0.5 3 § Concentrations of NH4 + and 1004 in 4 or 5 respire­ c.J • meters containing Stauroteutbis syrtensis were distin­ '--~ UU OJ guishable from chanqos in controls (Table 4). How­ 0 -.J -0.5 ever, most concentrations were near detection limits • • regardless of holding times. A small individual, Octo­ -1.0 /• pod 6 (Table 2), excreted 3 to 45 times as much NIL!" as -1.5 the other octopods (Table 4). With this individual in­ 0.0 0.5 1.0 1.5 2.0 2.5 cluded, the weight-specific and C-specific excretion Log1Q[WW (g)] rates for NH4 + decreased for larger S. syrtensis, with the curves explaining 92 to 96 '1'0 of the variation in the 1.5 L091O(C) =-0.9 + 1.2 x L091O(DW} c data (Fig. 4). Similar decreasing relationships ex­ 1.0 R2 =0.94, p < 0.001 plained 47 to 70 'X, of the variation in the PO/- data when the values recorded for Octopod 3 were ex­ 0.5 9 cluded (Fig. 5). This octopod was one of the largest 0 3 '--0 0.0 (Table 2), and it excreted more P04 - than predicted by OJ the model, perhaps due to an imperceptible injury. 0 -.J -0.5 • • Atomic ratios for O:N, O:P and N:1O, calculated -1.0 • from values measured during single experimental • runs, ranged from 11.01-365.83, 376.52-11471.99 and -1.5 1.03-135.84, respectively (Table 5). Removing Octo­ -0.5 0.0 0.5 1.0 1.5 pod 3, which had a relatively low rate of NH + excre- Log1Q[DW (g)] 4

Fiq. 2. St anrotenthis svrtensis. Lined!" roqression of loeJI,,-trdns­ Table 3. Stnuroteulhis svitensis. Weiqht-specilic and C-specific (DW, (WW, termed dry weiqht in g) (a) on wet weiqht in 9), (b) 0, consumption rates for cirrute octopods. WVV: wet weiqht. C ('onl,'nl (in q) on WvV. ilnd Ie) C content on DW for cirr ato DW: dry wuiqlu {J('I()!}()(J.s

consulIled~-·-·-~~- Octopod umol O 2 merits taken by micro-optodes were reliable measures 91WWhl qlDWh l q 'ChI of relative O 2 consumption, with micro-optodes consis­ tently yioldinq hiqher concentrations than the Winkler 0.043 0.918 4.631 tit rations (rnicro-optocle value = 1.35 x Winkler value, 2 0.22B 2.726 18.8Bl 3 0.072 1.565 9.013 F= 3541.35, df = 1,7, P < 0.001, R2 = 0.91). 4 0.107 2.354 25.7BB All octopods became quiescent and ventilated 5 0.092 2.108 19.44B calmly after an initial period of acclimation. All experi­ 6 0.098 1.851 11.830 ments yielded statistically siqnificant reqressions. with 7 0.243 2.963 16.363 0.031 0.576 5.363 O consumption in respirometers containinq octopods 8 2 9 0.194 3.192 14.220 being 1 to 2 orders of maqnitude qreator than O con­ 2 Mean 0.123 2.02B 13.949 surnption in controls. Steuroieutbis syrtensis consumed ± SE ± 0.026 ± 0.299 ± 2.327 5 to 35 'X, of the O 2 available at the start of the experi- 18 Aqual BioI 5: 13-22, 2009

0.3 0.15 NH excretion =4.1 x WW·16 a 0:, use =0.6 x WW-05 a 4 'j ,- R" = 0.95 .r: • R2 = 0.42 s: :s: • :s: 0.2 0 0.10 • ,-:s: ,-:s: Ol Ol 0 Ol E 0.1 2 0.05 • -r 2 I N • 0 • • Z 0.0 0.00 0 50 100 150 200 0 40 80 120 160 Wet weight (g) Wet weight (g)

4.0 2.0 02 use =2.1 x DW04 b • NH4 excretion = 0.9 x DW-1.6 b ,- R2 =0.25 ,- R2 =0.96 .r: 0 s: 1.5 ~ • ~ 0 • 0 'I OJ 2.0 Ol 1.0 0 Ol E ~ 2 2 -e- I 0.5 N • 0 • Z 0.0 0.0 • 0 4 8 12 0 2 4 6 8 Dry weight (g) Dry weight (g)

30 02 use =6.4 xC-os C 15 NH4 excretion = 0.3 x C-1.5 C R2 0.43 • = R2 = 0.92 'I ,- .r: • 20 .r: ,-o ,-o 10 Ol 0 Ol 0 Ol 10 2 E 5 2 I "" N 0 <:• • Z 0 0 • 0.0 0.5 1.0 1.5 2.0 2.5 0.0 0.5 1.0 1.5 Carbon content (g) Carbon content (g) Fig. 3. Stnuroteuthis syrtensis. Rates of 0". consumption ver- sus (a) WW, (b) DW, and (c) C content for cinate octopods. Fig. 4. Steuroteutbis syrtensis. Rates of NH.j' excretion ver- Values for Octopod 9 (grey circle) excluded from data used to sus (a] WW, (b) DW, and (c) C content for cinate octopods. fit the curve. Definitions as in Fig. 1 Definitions as in Fig. 1

Ta ble 4. Steutoteuthis svrtensi«. Weight-specific and C-specific NH4+ and po.?- excretion rates....-: data unavailable

Octopod -.---....---- >1~J NH.j' excreted------..--- fig PO.j"- excreted---- 1 1 s' WW h- g-1 DW hI g 1 WW h'' ~r' DW n' g' C h- _._...._._..._._------0.0005 0.0117 O.05BB .) 00144 0.4118 2B51B 0027B O.G049 3.484b

0.0229 0.5239 4.8335 0.0096 0.1802 1.1515

0.0191 0.3465 2.4 760 ± 0.0062 ±O.1101 ± O.B460 Jacoby et at: Distribution, behavior and metabolism of Stauroteutbls syrtensis 19

0.04 PO 4 excretion = 1.5 x WW-1.6 a Table 5. Stnurot.euthis svrteiisis. Ratios of oxygen (0) con­ 'I R2 = 0.54 sumed to nitrogen (N) and phosphorus (P) excreted. --.: data ..c • unavaiIable § 0.03 o 'I Octopod O:N O:P N:P OJ 0.02 • OJ 2> 1 1147UJ9 963.75 O~ 0.01 • 2 0.. 3 36:>B3 376.:>2 un 4 000 5 585.70 o 50 100 150 6 11.01 1495.55 135.84 Wet weight (g) 7 99.76 B 60.43 9 1.0 P04 excretion = 0.3 x DW-18 b Mean ± SE 134.26 ± 2978.70 ± 68.43 ± 'I R2 = 0047 ..c 0.8 79.3D 2131.82 67.41 ~ Without Octopod 3 0 0.6 o Mean ± SE 55.D7 ± 135.84 'I OJ • 25.68 OJ 004 2> • Without Octopod 1 -e- Mean ± SE 855.38 ± 245.56 0 0.2 0- • 0.0 0 2 4 6 8 son, Stauroteuthis svrtensis were composed of > 90 'i<, Dry weight (g) water, 3 to 7 % C, and 0.6 to 1.4 'X, N. In addition, the chemical composition of S. syrtensiswas more similar excretion = x 2 O to values reported for various gelatinous zooplankton 5 • P04 0.04 C- c R2 = 0.70 than to values reported for crustaceans or fishes 'I ..c 4 (Bailey et al. 1995). S. syttensis, various medusae and 0 0 ctenophores have water contents >90';10, C contents 'I 3 OJ <25% of DW, and N contents <5% of D\V. In contrast, OJ 2> crustaceans and fishes typically have water contents .., 2 dJO .r: contents >35'~!;), and N contents >5%. Thus, 0 \ 0- • the metabolic rates of S. syitensis would be expected to be similar to those of gelatinous zooplankton. 0 C-specific rates of O 2 consumption recorded for 0.0 0.5 1.0 1.5 Steuroteuthis svrtetisis were hiqher them values re­ Carbon content (g) ported for qelatinous zooplankton after scaling to a Fig. 5. Stnuroteuthis svriensis. Rates of PO."" excretion versus temperature of 4.5"C using a Q 10 of 2 (148 to 825 ul O 2 (a) WW, (b) DW, and (c) C content for cirratc octopods, Values s' C h' in the present study versus 1 to 181 pl O 2 s' for Octopod 3 (qrey circle) excluded from data used to fit C h- I in Bailey et el, 1995). In contrast, scaled, weight­ the curve. Definitions as in Fi~J. 1 specific respiration rates for S. svriensis were at the lower end of ranqes reported for cephalopods from 1 1 tion, arid Octopod 1, which had d relatively low rate of shallow and deep water (0.9 to 7.8 III O 2 9 WW h· in 1 1 PO/ excretion, yielded a sinqle value of 135.84 for the present study versus 0.3 to 190.2 ul O 2 9- WW h· N:P and mean ratios (± SE) of 55.07 ± 25.68 for O:N and in Seibel et al. 1997, Ddly &. Peck 2000, Seibel s: Chil­

855.38 ± 245.56 for O:P (Table 5). dress 2000). Rates of O 2 consumption for S. svitensis W("Te most similar to those reported for the vampire squid Vampyroteuthis internalis and 2 deep-water DISCUSSION octopods, Japetella heuthi and J. diaphana (1.9 to

2.4 ul O 2 s' WW rr', 3.5 pI O 2 s' WW h": and 5.4 to 1 Water (73 to 87 '/\,) and protein (8 to 20 %) represent 19.4 ul O 2 s' WW h- ; Seibel et al. 1997). The similar­ the primary components of cephalopod bodies, which ity between the metabolic demands of S. syrtensis and yield estimates of 4 to 10 % C and 2 to 4 % N relative to V. internnlis rnav be related to the replacement of WW (Croxall & Prince 1982, Krzynowek & Murphy visual identification and pursuit of prey with a more 1'lH7 "doltschdniv'/skyj & S('nlfnens 2(00). 1n rornp.ui- passiv« strdte~JY. It has been hypothesized that both 20 Aquat BioI 5: 13-22, 2009

speCIes lise bioluminescence to lure prey (Childress & Converting O 2 consumption to C consumption by Mickel 1985, Johnsen et al. 1999, Collins & Henriques applying a respiratory quotient of 0.8 yielded estimates 2000, Seibel et al. 2000, Seibel &. Carlini 2001, Robison of metabolic demand expressed as 'X, body C d-' that 1 et al. 20(3). In addition to differential activity, some of ranged from 0.11 to 0.59% d ..· , with a mean (± SE) of the observed differences in O 2 consuurption may be 0.32 ± 0.05 % (Table 6). Examinations of gut contents 1 e~lclt(:d to alloiuctr!c scalin~J, with larger animals con­ from Steuroieuthis syrtensis expanded on previous sliming proportionally less 02, as observed in the pre­ reports that the octopods feci on unidentified copepods sent and previous studies (e.g. Seibel et al. 1997). An­ (e.g. Johnsen et al. 1999) and on the hypothesis that other consideration is that rates of O 2 consumption mucus secreted by buccal secretory glands entrapped measured at in situ pressures would be expected to be prey that were then handled by the cirri (Vecchione &. higher than the rates measured at sea level in the pre­ Younq 1997). In this case, only Celnnus Iinniarchicus sent and other studies (Bailey et al. 1994,1995). Previ­ was found in the stomachs of S. syrtensis, with the con­ ous comparisons and those in the present study are clition of the prey indicating that they were swallowed rdatl~d 10 mo.rsurcruunts mudo at surface pressures. whole. In addition, C. tiintuuchicus captured in the NIl~ + and P04 :1, excretion rates for Stauroteuthis svr­ canyons during September 2004 had accumulated tenSJS were low. The rates were at least an order of lipid stores (Miller et al. 1998). which S. syrtensis could magnitude lower than those reported for 2 species of have assimilated and stored, as reported for a species ctenophores, a trachyrnedusan and a benthopelagic of Opisthoteuihis (Rosa et al. 2(05). and eventually holothurian, i.e. 0.22 to 9.67 )1g NHrN s' C h' and metabolized to produce the observed O:N ratios. ~g I 0.02 to 1.58 P04 -1' g" C h- recorded in the present Converting the C requirements of S. syrtensis to daily study versus 55.4 to 1 389.5 )1g NH4-N s' C h" and maintenance rations by assuming a contribution of

11.6 to 443.5 pg P04 -P g-I C h-' reported in Bailey et al. 0.234 mg C ind."' of C. tinnuircbicus yielded rations (1994). In addition, rates of NH/ excretion for S. syr­ of 1.3 to 30.1 indo d-I, with a mean (±SE) of 6.7 ± tensis were approximately 3 orders of maqnitude less 3.1 indo d· 1 (Table G). Thus, the metabolic demands of than rates reported for the Antarctic octopod Perele­ relatively inactive S. svrtensis, which often float pas­ done ciuucoti and the shallow-water octopod Octopus sively according to observations made during the pre­ ocellatiis: 0.04 to 1.51 pg NH4-N s DW h-' and 0.002 sent and previous studies (Vecchione & Young 1997, to 0.080 pg NHrN )19 1 WW hI in the present study Collins et a1. 2(02), would be met by the prey available I versus 2521.2 pg NIl4,N g-I DW h- in Daly & Peck in <1 m' of Welter, given the mean abundance of C. fin­ 1 l2000j und 3 to 40 pl) NIL1-N ]Tg WW rr' in Segawa & morchicus measured across all 3 canyons in 2002. Nomoto (2002). The unavoidable need to store the The in s-itu observations made during the present samples before analysis may have resulted in lower study confirmed and expanded on knowledqo of the concentrutions. but excretion rates should have re­ distribution of Stnuroteutbis syrtensis. This species has mained valid unless the loss of NH4+ or 1'04:1- was often been captured in bottom trawls (Collins & Hen­ unequal across samples. The relatively low rates of N riques 2(00), and the octopods observed and captured excretion also could be related to storage of NH/ or durinq our study were, on average, approximately other nitrogenous cations as an evolutiondry adapter­ tion to increase buoyancy (Seibel et al, 2(04). Table 6. Sinuroteutliis svrtensis: Metabolic demand, calcu­ The relatively low excretion rates translated into rel­ latcd from O 2 consumption usinq an assumed respirulory quo­ tient of 0.8, and Inferred maintenance ration based on the dS­ atively hiqh atomic ratios compared to values reported surnption that d single Calanus Iinmnrcnicus contained for other zooplankton. The O:N and 0:1' ratios for Stall­ 0.234 rng of C roteiithis svrtensis (11 to 366 and 376 to 11 472, respec­ tively) typically WPIe higher than those reported for d Octopod Metabolic demand Maintenance ration l variety of Antarctic zooplankton (7 to 20 and 43 to 304, ('X, body C dll (no. of copepods d ) respectively; Ikeda &. Mitchell 1982) and 2 species of ctenophores, a trachymedusan and a benthopelagic 1 0.11 32 holothurian (9 to 24 and 50 to 317, respectively; Bailey 2 0.43 29 3 0.21 10.4 (~t 1 al. CJCJ4) In addition, the O:N ratios for S. syrtensis 4 0.59 2.3 were hiqhor t ha n those reported for Octopus vulgaris 5 0.45 3.5 (3 to 15; Katsanevakis et al. 20(5). Given the observed 6 0.27 1.3 O:N ratios. S. syrtensis seemed to metabolize lipids 7 CU8 5.2 8 0.12 1.5 (Mayzaucl & Conover 1988). In addition, the high O:P 9 0.33 30.1 and N:P ratios indicated that most octopods were not Mean 0.32 6.7 & Ieekinq phosphorus clue to injury (Mayzaud Conover ± SE ± 0.05 ± 3.1 1988). Jacoby e l al.: Distribution, behavior and metabolism of Stnuroteuthis syrtensis 21

100 m off tho bottom during the day and at night. The Acknowledgements, We greaLly appreciate the assistance pro­ ecological importance of the statistically significant vided by the crews of the RV 'Seward Johnson I' and 'Seward Johnson II', the crews of the 'Johnson-Sea-Link' submersibles difference in mean depth between daytime and night­ and all participants in tho research cruises, The study was sup­ time sightings remains uncertain, This difference rep­ ported by a grant to M,J,y' from the National Science Founda­ resented approximately 4 'X, of the total average depth tion (NSF-0002493), the European Project Euroge1, and the of the water column, Observations of up to 5 octopods United Stales Department of Agriculture Current Research Information System Project FLA-FAS-04611. This work repro­ 111 d 4UU Ill' liuld 01 VJeW indicated that trawl surveys sents HBOl/FAU Contribution Number 1723, yielding octopod abundance estimates of 8 to 9 ind. krn? swept area may have integrated small-scale LITERATURE CITED patches of octopods (Collins et al. 2(01), Although octopods may have sensed the sub­ American Public Health Association (1989) Standard methods mersible before they were sighted, in situ observations for the examination of water and wastewater: including bottom sediments and sludges, 17th edn. American Public revealed that many individuals drifted in a 'sleeping Health Association, Washington, DC mode,' with their bodies contracted into a relatively )W-- Bailey TC, Tones JJ, Youngbluth MJ, Owen CP (1994) Effect compact ball and their eyes hooded, In this posture, the of decompression on mesopclaqic gelatinous zooplankton: octopod was difficult to distinquish from floating a comparison of in situ and shipboard measurements of metabolism, Mar Ecol Prog Ser 113: 13-27 debris. This quiescent behavior was not exhibited by » Bailey TC, Youngbluth MJ, Owen CP (1995) Chemical com­ captive octopods. In response to disturbance caused by position and metabolic rates 01 gelatinous zooplankton tho submersibles, Stauroieutbis svrtensis inflated its from midwater and benthic boundary layer environments web complex and exhibited the ballooning behavior off Cdfle Hatteras. North Carolina, USA, Mar Ecol Pr09 Ser 122:121134 noted previously (Vecchione & Young 1997, Johnsen et Boletzky SV, Rio I'd, Roux M (1992) Octopod 'ballooning' aL 1999, Collins ct at. 2(02), Thus, observations in the response, Nature 356: 199 present study supported the hypothesis that these Childress JJ, Mickel 'IJ (1985) Metabolic rates of animals behaviors may function as an alarm response to deter from the hydrothermal vents and other deep-sea habitats, or confuse predators, such as Cuvier's beaked whales Bull Bioi Soc Wash 6:249-260 » Collins MA (2002) Cirrate octopods from Greenland and Ziphius cavirosttis and blue sharks Priouace qleuca Iceland waters, J Mar BioI Assoc UK 82:1035-1036 (Vecchione & Young 1997, Johnsen et al, 1999, Santos )W-- Collins MA, Henriques C (2000) A revision of the family et al. 2001, Collins et at. 2002, Kubodera et aL 2(07), Stauroteuthidae (Oclopoda: Cinala) with redescriptions of Observations also indicated that slow sculling of the Stnuroteutbis svrieiisis and S, qilchristi. J Mar Biol Assoc peired fins, medusoid contractions of the web, and UK BO:685-697 Collins MA, Villemueva R (2006) Taxonomy, ecology and rapid Iin sculling were similar to patterns of locomotion behaviour of the cinate octopods, Oceanogr Mar Bioi reported lor another deep-water cephalopod, Vampy­ Annu Rev 44:277-322 roteutliis internalis (Seibel et al. 1998). S, svitensis ~ Collins MA, Vall C, Allcock L, Thurston MH (2001) Distribu­ seemed to employ this sequence of behaviors in tion of deep-water benthic and bentho-pelagic cephalo­ pods from the north-east Atlantic, J Mar Biol Assoc UK response to increased levels of disturbance, The be­ 81:105-117 haviors of S, svrteiisis also resemble those described Collins M, Young RE, Vecchione M (2002) Steuroteuthis for other cirrato octopods (Boletzky et al. 1992, Hov­ syrtensis Verrill, 1879, Available al: http.z/tolweb.orq/ land 1992, Villanueva et al. 1997), Stauroteuthis_syrtensis/20187/2002,01,30, (Accessed on In summary, the results of the present study confirmed 17 January 2(09) Croxall JP, Prince PA (1982) Calorific content of squid that Stauroteuthis svriensis is a deep-water species that (Mollusca: Cephalopoda), Br Antarct Surv Bull 55:27 --31 often lives near the bottom, The octopods typically )W-- Daly HI, Peck LS (2000) Energy balance and cold adaptation floated passively, and they responded to increasing dis­ in the octopus Paieledone chnrcoii. J Exp Mar Biol Ecol turbanro by inflating I heir webs and emplovinq progres­ 245:197-214 Hovland M (1992) Balloon response explanation? Nature 357: sively faster modes of locomotion to escape, S, svrtensis 119 fed on the copepod Calanus tinmarchicus, with relatively Ikeda 'I, Mitchell AW (1982) Oxygen uptake, ammonia excre­ few prey needed to meet their basal metabolic demands, tion and phosphate excretion by krill and other Antarctic In qeneral, the r hemk-al content of S, svttetisis was more zooplankton in relation to lheir body size and chemica] similar to gelatinous zooplankton than to more muscular composition, Mar Biol 71:283--298 )W-- Johnsen S, Balsr,r EJ, Fisher EC, Widder EA (1999) Biolumi­ cephalopods, but its O 2 consumption was greater than nescence in the deep-sea cinate octopod Steurot.eutliis that of gelatinous zooplankton and similar to other deep­ syrlensis Venill (Mollusca: Cephalopoda), BioI Bull 197: water cephalopods that have been reported to be 26--39 ambush predators, In addition, S, svitensis excreted ~ Katsanevakis S, Stephanopoulou S, Milieu H, Moraitou­ l Apostolopoulou M, Verriopoulos C; (2005) OXYgen con­ relatively little NII + or P0 : .., and the octopods seemed 4 4 sumption and ammonia excretion of Octopus vulgaris to catabolize lipids, which could have boon derived from (Cephalopoda) in relation to body mass and temperature, C, tinniarchicus. Mar Bioi 146:725-732 22 Aquat BioI 5: 1322, 2009

Krzvnowuk J. Murph v J (1987) Proximate composition, enerqy. Seibel FlA,Tlwusen EV, Childress JJ (1998) Fliqht ot the vam­ t.utv dcid, sodium, dnd cholesterol contenl of finfish. shell­ pire: ontoqenet.c qail-transitioll in Vampyroleuthis in­ fish, and fheir products. NOAA Tech Rep 55 Ierunlis (Cephalopoda: Vampvromorpha). J Exp BioI 201: >- Kubodera T, Watanabe H, Ichii T (2007) Feedinq habits of 24132424 the blue shark, Prionnce g]dUCd, and lemon shark, Lemtie Seibel BA. Theusen EV, Childress JJ (2000) Liqhl-Iirnitation ditropis, in the transition reqion of the western North on predator-prey interactions: consequences for meta­ Pacific Rc'v Fish Bioi Fish 17: 111-124 bolism and locomotion of deep-sea cephalopods, Biol Bull >- Mayzaud P, Conover RJ (1988) O:N atomic ratio as a tool to 198:284--289 describe zooplankton metabolism, Mar Ecol Prog Sor 45: liw Seibel BA. Coffredi SK, Thousen EV, Childress JJ, Robison 289-302 BH (2004) Ammonium content and buoyancy in midwater Miller (:B, Morgan CA, Prahl FG, Sparrow Mil. (199B) Storaqe cephalopods. J Exp Mar BioI EcoI313:375-387 lipids of the copepod Cnlanus Iinmnrchicus from Georges Strickland JO, Parsons TR (1972) A practical handbook of Bank and the Gulf of Maine. Lirnnol Oceanoqr 43:488-497 seawater analysis. Bull Fish Res Board Can 167 ~ Moltschaniwskvj NA, Semmens JM (2000) Limited use of Tietze RC, Clark AM (1986) Remotely operated tools for stored ener~1Y reserves for reproduction by the tropical undersea vehicles, In: McGuiness T (ed] Current prac­ louqund sq uid 1']1010]01190 sp. J Zool (Loud) 251:307 -313 tices and new technology in ocean e nqineerinq. Ameri­ ... Robison BH, Reisenbichfer KR, Hunt JC, Haddock SHD (2003) can Society of Mechanical Enqincers. New York, Liqht production by the arm tips of the deep-sea cephalo­ p 219--223 pod Vnuipvroteuttiis inteinnlis. Bioi Bull 205: 102 ..·109 liw Vecchione M, Galbraith J (2001) Cephalopod species col­ >- Rosa R, Pereira J, Nunes M (2005) Biochemical composition of lected by deepwater exploratory Iishinq off New Enqland, cephalopods with different life hislory strataqies, with Fish Res 51:385-391 spe-cial rderence to a qiant squid, Arcliitcuthis sp. Mar Vecchione M, Pohle G (2002) Midwater cephalopods in the BioI 14f:i:739-751 western North Atlantic Ocean off Nova Scotia. Bull Mar Santos MB, Pierce CJ, Herman J, Lopez A, Guerra A, Mente Sci 71 :883-892 E, Clarke MR (2001) Feeding ecoloqy of Cuvier's beaked Vecchione M, Young RE (1997) Aspects of the functioned whale (Ziphius cavirostris): a review with new inforrna­ morphology of cirrate octopods: locomotion and Iecdinq. Lion on the diet of this species, J Mar Bioi Assoc UK 31: Vie Mllleu47:101-110 tiB7·· ti94 liw Villanueva R. Seqonzac M, Guerra A (1997) Locomotion Se~Jawa S, Nomoto A (2002) Laboratory qrowth, Ieedinq, modes of deep-sea cirrate octopods (Cephalopoda) based ox yqen consumption and ammonia excretion of Octopus on observations from video recordinqs on the Mid-Atlantic oeellatlis. Bull Mar Sci 71 :801· 8l:J Ridqe. Mar Bioi 129:1I:3-122 Seibel BA, Carlini DB (2001) Metabolism of pelaqic cephalo­ Welzel FG, Likens GE (2000) Limnoloqical analyses, 3rd edn. pods as a function 01 habilat depth: a reanalysis usinq Springer, New York phvloqeneticall y independent contrasts. Biol Bull 201: 1-5 Younqbluth MJ (1984) Manned submersibles and sophisti­ ... Seibel BA, Childress JJ (2000) Metabolism of benthic octo­ cated instrumentation: tools for occanoqraphic research. pods (Cephillopoda) as a function of habitat depth and In: Proceediriqs of Subtech 83 Symposium. Society for oxyqen concentration, Deep-Sea Res 1 47:1247-12tiO Underwater Technoloqy, London, P 335-344 )i> Seibel BA, Theusen EV, Childress JJ, Gorodezky LA (1997) ~,. Younqbluth MJ, Kremer P, Bailey TG, Jacoby CA (1988) Decline in palaqic cephalopod metabolism with habitat Chemical composition, metabolic rules and feeding be­ depth re[lects differences in locomotory efficiency. Biol havior of the midwaler ctenophore Benhocvroe Iosteri. Bull 192:262-278 Mar BioI 98:87--94

Editorial responsibility: Hens Heinticli Janssen, Submitted: September 29, 200B; Accepted: November 28, 2008 (lid, -nciort/Lutu», CermdllY Proois received hom authotts]: .tetiuary 21,200.9