Journal of Marine Systems 88 (2011) 563–567

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Journal of Marine Systems

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Naturally occurring bioluminescence on the deep-sea floor

Jessica Craig ⁎, Alan J. Jamieson, Philip M. Bagley, Imants G. PriedeUniversity of Aberdeen, Oceanlab, Main Street, Newburgh, Aberdeenshire, AB41 6AA, UK

⁎ Corresponding author. Tel.: +44 0112 274440; fax:E-mail address: j.craig@abdn.ac.uk (J. Craig).

0924-7963/$ – see front matter © 2011 Elsevier B.V. Aldoi:10.1016/j.jmarsys.2011.07.006

a b s t r a c t

a r t i c l e i n f o

Article history:Received 19 January 2011Received in revised form 6 July 2011Accepted 10 July 2011Available online 22 July 2011

Keywords:Spontaneous bioluminescenceNaturally occurring bioluminescenceBioluminescent zooplanktonVisual environmentDeep seaLow-light cameraMid-Atlantic Ridge

In the deep sea, bioluminescence that is not stimulated by the observer is estimated to be extremely low.Observations of naturally occurring bioluminescence, using an ultra-low-light video camera, at a solitary rockpopulated with sessile fauna revealed bioluminescent activity was 155 times higher than predictedbackground levels at 2000–3000 m. These findings, from the Mid-Atlantic Ridge (49.022°N, 27.693°W),suggest that, at depths below the penetration of sunlight, complexity in the physical environment mayinfluence the visual environment, with potential effects on the behaviour of mobile deep sea fauna, promptinga reappraisal of the visual environment in the deep sea.

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© 2011 Elsevier B.V. All rights reserved.

1. Introduction

In the deep sea, below the penetration of sunlight, biolumines-cence is themain source of light where it is used for defence (Haddockand Case, 1994, 1999; Robison et al., 2003), offence (or ‘luring prey’;Robison et al., 2003; Haddock et al., 2005), and for communication(Rivers and Morin, 2008; Woodland et al., 2002). The biochemistry,physiology and function of bioluminescence at species levels isrelatively well known for many deep-sea taxa (reviewed in Haddocket al., 2010), however the rate at which the production of biologicallight occurs naturally, whether pelagic or benthic, remains unre-solved. This is partly due to the tendency to use mechanical stim-ulation for large-scale studies on the distribution of bioluminescentorganisms. This technique can be executed using either flow throughpump bathyphotometers (Clarke and Hubbard, 1959; Clarke andKelly, 1965; Herren et al., 2005; Widder et al., 2003), low-lightcameras filming a mesh screen traversing horizontally or verticallythrough the water column (Widder et al., 1989; Priede et al., 2006respectively), or using stationary arrays of photomultipliers recordingevents as they impact the array in the surrounding currents (Aguilarand The ANTARES Collaboration, 2006). To date these techniques haveproduced a large scale interpretation of the distribution of pelagicbioluminescent organisms across much of the Mediterranean Sea(Craig et al., 2009, 2010, 2011; Priede et al., 2008), Northeast Atlantic

(Gillibrand et al., 2007a) and over the Mid Atlantic Ridge (Heger et al.,2008; Piontkovski et al., 1997).

In the deep-sea benthic environment, bioluminescence studieshave typically favoured artificial stimulation of bioluminescence usingbaited rather than mechanical methods (Gillibrand et al., 2007b;Heger et al., 2007; Priede et al., 2006; Widder, 2002). In addition toother sensory cues such as chemoreception (Bailey and Priede, 2002;Lokkeborg et al., 1995; Sainte-Marie and Hargrave, 1987), mechano-reception (Klages et al., 2002) noise and hydrodynamic disturbance(Wilson and Smith, 1984), bioluminescence is thought to provide animportant cue in the acute localising of food-falls on the deep-seafloor (Priede et al., 2006). Bioluminescent activity in the presenceof food-falls is known to vary greatly with depth and substrata(Gillibrand et al., 2007b; Heger et al., 2007) and although it representsa natural response to the presence of food-falls, it does not representthe visual environment in the absence of such stimuli. Variations innaturally occurring bioluminescence have the potential to mask orobscure this sensory cue.

Heterogeneity in the visual environment is an unexplored aspect ofthe deep sea benthic environment and thus the frequency of naturallyoccurring bioluminescence on the deep-sea floor has remained some-what of an enigma. It is currently estimated that un-stimulated back-ground rates are extremely low (Priede et al., 2006; Widder, 2002);predicted to be 1 event h−1 in the field of view of a sea floor camera at2000–3000 m depth (Gillibrand et al., 2007b). Bioluminescencenot stimulated by the observer is usually referred to as ‘spontaneous’(Widder et al., 1989). However, this term is misleading as the bio-luminescence may result from a stimulus unknown to the observer;instead we refer to naturally occurring bioluminescence.

564 J. Craig et al. / Journal of Marine Systems 88 (2011) 563–567

Here we report observations of naturally occurring biolumines-cence on the deep-sea floor of the Mid-Atlantic Ridge (2381 m), withobservations from baited experiments for comparison. We investigatethe significance of this finding in relation to the complexity of the seafloor on the Mid-Atlantic Ridge.

2. Materials and methods

2.1. Quiescent bioluminescence observations

An ultra low light ICDeep (Image Intensified Charge CoupledDevice for Deep Sea research) camera (minimum faceplate sensitivity5×10−7 lux) was mounted on the tool tray of the ISIS RemotelyOperated Vehicle (ROV) (DIVE#178, 27/06/2010; Table 1). The ROVwas brought to rest on the sea bed downstream of a solitary rock(0.6×0.5×0.5 m) at 2381 m depth at a site on the east side of theMid-Atlantic Ridge (49.022°N, 27.693°W). The rock was populated bystalked crinoids, sponges and other sessile fauna and surrounded bysoft sediments. The ROV lights were switched off and after 8 minsettling time the ICDeep was used to film the rock in quiescent con-ditions for 10 min. The footage obtained from this method (and theother deployment modes) was digitally recorded in MPEG4 format.The footage was played back and the time of occurrence and eventduration and type were noted for each event. The size of the rock andassociated fauna from this footage was digitally calibrated from the insitu ROV laser scales (2 dots 0.1 m apart).

2.2. Baited experiment bioluminescence observations

The ICDeep lander (an upgraded version of that described in Priedeet al., 2006) was deployed eight times on the Mid-Atlantic Ridge atdepths ranging from 1659 to 2622 m (Table 1). The lander wasconfigured with the ICDeep camera mounted vertically 0.8 m abovebait (Scomber scombrus, 500 g) attached to a metal arm resting on thesea floor, with a field of view of 0.8×0.65 m (0.52 m−2). A red LEDwas used to illuminate the scene at specified intervals to enableobservation of megafauna present. Red light, not visible to most deepsea animals, was used to minimise behavioural artefacts and damageto eyes (Widder et al., 2005). The camera was programmed to capturevideo for 2 min 30 s with no artificial light, followed by 15 s with thescene illuminated. This sequence was repeated for a 1 h period at all

Table 1Deployment details and mean rate of bioluminescent events (min−1) for the quiescent anabove the seafloor.

Date Depth (m) Latitude (°N

Quiescent bioluminescence observations (ROV)1 27/06/10 2381 49.022

Baited bioluminescence observations (lander)1 07/08/09 1659 49.0382 10/08/09 2438 49.0253 17/08/09 1880 49.0374 22/08/09 2622 48.7325 26/08/09 2319 53.9786 28/08/09 2552 53.9897 31/08/09 2539 53.9498 02/09/09 2501 54.075

Date Depth (m) Latitude (°N) Longitude (°W) Dista

Near-bed (5 m altitude) horizontal transect (ROV)1 23/06/10 2467 49.120 27.833 1722 23/06/10 2738 49.103 27.836 2003 26/06/10 2755 49.021 27.722 196

stations. The field of view from the baited lander was calculateddigitally using the bait arm as a calibration scale.

2.3. Measurement of bioluminescent sources at 5 m altitude

The ICDeep camera was mounted on the tool tray of the ISIS ROV(Table 1). Amesh (0.43×0.43 m;0.18 m−2)was placed0.5 m in frontofthe camera using the manipulator arm. The ROV moved forwards atspeeds ranging from 0.2 to 0.5 m s−1. Bioluminescent sources thatimpacted on or passed through the mesh were stimulated to lu-minesce. These flashes were recorded on video during three ~200 mtransects at 5 m above the sea bed. During video replay each flash,corresponding to a single bioluminescent organism, was counted. Thedensity of bioluminescent zooplanktonwas calculated from the volumeof water sampled during the 200 m transect.

2.4. Sea floor rock density transects

High-Definition (HD) videodatawere collectedusing the ISIS ROV toassess the density of outcropping rocks on the sea floor (Table 2). In thevicinity of the quiescent bioluminescence observations, two transectswere performed on relatively flat slopes of 10°±2 S.D., and two onsteeper slopesN30°. For all transects the ROV travelled at a constantspeed of 0.13 m s−1 for a distance of 500 m on a bearing approximatelyparallel to the ridge axis. On the 10° slope transects a verticallymountedHD video camera was used with two parallel lasers (0.1 m apart) andsampled an area of 1000m2. On the N30° slopes a horizontallymountedHD camera was used with parallel lasers (0.1 m apart). The ROVtravelled sideways during these transects, however, the topographiccomplexity of these slopes caused deviation from this path, so an exactcalculation of the sampled area could not be made. The maximum areasampled was 1000m−2 and the minimum was 550 m−2.

The video was analysed to identify outcropping rocks that have thepotential to stimulate bioluminescence from collisions by organismsadvected by the impinging current. Individual rocks (of size≥0.1 m×0.1 m)were counted in areaswhere thepredominant substratewas sediment. In areas with a surface area of rock N25%, individual rockswere not counted and the areawas classed as rocky substrate with somesediment cover. On the N30° slope transects mean rock densities werecalculated using the maximum and minimum sampled area.

d baited observations and mean density of bioluminescent zooplankton (m−3) at 5 m

) Longitude (°W) Mean rate of bioluminescentevents (± S.D.) (min−1)

27.693 3.1

27.788 2.2±2.027.788 1.7±1.127.926 2.0±1.628.646 1.1±1.136.102 1.8±2.336.135 0.6±1.234.056 0.4±0.834.163 0.7±0.6

nce (m) Bearing Speed (m.s−1) Mean density of bioluminescentzooplankton (± S.D.) (m−3)

323° 0.44 12.0208° 0.46 10.4188° 0.23 13.5

Table 2ROV video transects details with rock substrate ratio (%) and mean rock density (rocks 1000 m−2).

Sea floor rock density transect (ROV)

Transect Date Depth (m) Slope Latitude (°N) Longitude (°W) Distance (m) Bearing Rock substrate(% area)

Mean rock density(±SD) (1000 m−2)

1 26/06/10 2563 N 30° 49.021 27.685 500 18° 65 177±1322 26/06/10 2541 N 30° 49.015 27.685 500 19° 83 118±403 26/06/10 2601 10±2° 49.017 27.707 500 19° 3 14 26/06/10 2646 10±2° 49.014 27.709 500 17° 0 0

565J. Craig et al. / Journal of Marine Systems 88 (2011) 563–567

3. Results

Sea floor surveys in this region, using the ISIS ROV revealed thatmuch of the area is draped in fine sediment punctuated by rockyoutcrops and cliff faces with little conspicuous life. The exceptionswerecertain exposed buttresses and rocks where sessile fauna formed‘garden-like’ assemblages. One such rock (0.6×0.5×0.5 m) surroundedby soft sediments and populated by stalked crinoids, sponges and othersessile fauna was observed (Fig. 1A). The rock and associate fauna wasfirst observed in HD using conventional white lights on the ROV,followed by quiescent filming with the ICDeep camera. During tenminutes of quiescent filming thirty-one naturally occurring biolumi-nescent eventswere observed (Fig. 1B), equivalent to 3.1 events min−1.

These bioluminescent events consisted either of trains of smallflashes, a single continuous flash or extrusions of luminescent material(Fig. 1C). The mean duration of the observed bioluminescent events

Fig. 1. (A) Solitary rock with stalked crinoids, sponges, corals and brittle stars.(B) Location of bioluminescent events (white circles) superimposed on illuminatedview of the rock from the ICDeep camera. (C) Example bioluminescent events (samescale as background image).

was 5.5 s±6.7 S.D. (Fig. 2). Seventy-seven percent of the biolumines-cent events occurred on the attached non-bioluminescent crinoids,Anachalypsicrinus nefertiti.

The density of bioluminescent zooplankton in the water column at5 m above the sea bed in the region was measured as 12.0, 10.4 and13.5 m−3 at 2467, 2738 and 2755 m respectively (overall mean den-sity of bioluminescent zooplankton=11.96 m−3±1.52 S.D.).

The frequency of bioluminescent events observed by the baitedcamera ranged from 0.4±0.8 to 2.2 min−1±2.0 S.D. (see Table 1,Fig. 3). Linear regression was applied to the mean flash rates obtainedfrom each deployment to assess the significance of an inverse depthtrend in bioluminescence, as previously reported by Gillibrand et al.(2007b). Linear regression was chosen as our bioluminescenceobservationswere taken over a 1000 mdepth rangewhichwas deemedtoo truncated to detect a logarithmic trend as identified by Gillibrandet al. (2007b) (shown in Fig. 3) whose measurements ranged overalmost 4000 m. A significant inverse depth trend in bioluminescentactivity was found (rate of bioluminescent events (min−1)=5−(1.6×10−3×D), where D is depth (m), R2=0.61, pb0.05).

The sea floor ROV transects revealed that on theN30° slope, rockysubstrate comprised83%of the area sampledduring transect 1 and65%ofthe area during transect 2. In the remaining areas of sediment substrate,the overall mean density of outcropping rocks (≥0.1 m×0.1 m) ontheN30° slopeswas 148 rocks 1000 m−2±96 S.D., allowing for the errorin area sampled. On the 10° slopes, rocky substrate comprised 3% oftransect 3 andwas absent from transect 4. The overall mean outcroppingrock density on the sediment substrate fromboth transectswas 0.5 rocks1000 m−2±0.7 S.D.

4. Discussion

Despite the prevalence of bioluminescent capability amongst deepsea fauna, previous studies have reported that few bioluminescentevents occur in the absence of artificial stimulation, both from mid-water submersible observations (Widder et al., 1989) and from non-baited benthic lander deployments (Gillibrand et al., 2007b; Priedeet al., 2006). Interpolating between observations in the absence of baitfrom the Gillibrand et al. (2007b) study, the rate of naturally occurringbioluminescent events is predicted to be 0.02 min−1 at 2400 m depth(Fig. 3). This is an order of magnitude lower than the predicted rate ofartificially stimulated bioluminescence events of 0.2 min−1 in thepresence of bait at the samedepth (Gillibrand et al., 2007b). The resultsof the current study predict a rate of bait stimulated bioluminescenceevents of 1.2 min−1 at this depth. It should be noted that the ISITcamera used in the Gillibrand et al. (2007b) study is less sensitive thanthe ICDeep camera used in our study, so the 6-fold difference inobservations between the two systems likely represents biolumines-cent emissions from fainter sources undetected by the ISIT camera(Craig et al., 2011). However, the rate of naturally occurring bio-luminescent events observed in this study (3.1 min−1) equates to arate 155 times higher than the non-baited ISIT observations. Takinginto account the increased sensitivity of the ICDeep camera, this stillrepresents an exceptionally high rate of naturally occurring biolumi-nescent activity compared to previous observations.

Fig. 2. Timing and duration of bioluminescent events (dark horizontal bars) during 10 min of quiescent filming with the ICDeep camera at the rock. Duration of each event includesfull activity cycle of one organism including periods with and without emitted light.

566 J. Craig et al. / Journal of Marine Systems 88 (2011) 563–567

Seventy-seven percent of the bioluminescent events on theisolated rock occurred on the attached non-bioluminescent crinoids,Anachalypsicrinus nefertiti. These crinoids are passive filter feeders(Meyer, 1982) and it is likely that these bioluminescent events were thedefensive reactions of zooplankton trapped on or colliding with thefiltration arms. During filming the impinging current was 0.12 m s−1.Priede et al. (2008) proposed a relationship to predict the bioluminescentflash rate produced by advected organisms colliding with a fixedstructure. The mean density of bioluminescent zooplankton in thewater column at 5 m above the sea bed was 11.96 m−3. Assuming acrinoid arm length of 0.1 m and a zooplankton diameter of 5 mm,collisions between one crinoid and advected zooplankton would beexpected to produce a rate of naturally stimulated bioluminescent eventsof 2.9 min−1, assuming all collisions resulted in a flash (Priede et al.,2008). There were 6 crinoids in view during quiescent observationswhich would produce a predicted bioluminescent event rate of17.1 min−1, considerably higher than the observed rate of 3.1 min−1.This suggests that the density of bioluminescent zooplankton and currentspeed are more than sufficient to explain the observed rate ofbioluminescent flashes even if not all collisions resulted in a biolumines-cent reaction. Hartline et al. (1999) found contact was not alwaysnecessary to mechanically stimulate bioluminescence. They found that ahydrodynamic disturbance of 5.5 mm s−1 was sufficient to elicitbioluminescence in a copepod (Hartline et al., 1999). Although thisthreshold stimulusmaybehigher for other species, there appears tobenoneed to invoke any active behaviour either by the copepod or the crinoid.

To assess the influence naturally occurring bioluminescence mayhave in the deep sea environment, it is important to consider thedistance at which bioluminescent events are visible in the deep seaenvironment. Warrant and Locket (2004) predicted that an averagebathypelagic fish is likely to be able to detect a typical flash of 1010

photons at a distance up to 100 m. However, this value was calculatedfor ideal conditions. Several factors are likely to reduce this distance,including a flash of lower intensity, reduced transparency of the waterfrom suspended material, smaller pupil size of the observer as well asthe spectral and temporal sensitivity of the observer (Turner et al.,2009). Bioluminescence is a persistent feature at deep-sea neutrinotelescope installations, where advected zooplankton impinge on the

Fig. 3. Bioluminescent events (min−1) for baited camera observations (closed dots;linear regression (bioluminescent events (min−1)=5–1.6×10−3×Depth (m),R2=0.61, pb0.05)) and quiescent observation (open dot), from observations withthe ICDeep camera at the Mid Atlantic Ridge. Dotted line shows depth trend ofbioluminescent events at bait and dashed line shows the depth trend in the absence ofbait, both observed using an ISIT (Intensified Silicon Intensifier Target) camera in theNE Atlantic Ocean (from Gillibrand et al., 2007b).

underwater structures (Amram and The ANTARES Collaboration,2000). It is likely therefore that features on the seafloor, such as rocksthat protrude into the flow of water, would produce a similar effect.

On the Mid-Atlantic Ridge, areas of rocky substrate are likely toprovide a continual natural stimulus for bioluminescence. Addition-ally, bioluminescent events are likely to be stimulated by protrudingrocks located in areas of sediment.We observed amean density of 148rocks 1000 m−2±96 S.D. on sediment slopesN30°. Assuming an idealthreshold detection radius of 100 m (Warrant and Locket, 2004) therewould be 4650 rocks ±3015 S.D. with the potential to stimulatebioluminescence within visible range of a stationary fish (Fig. 4). Evengiven a more conservative threshold detection radius of 5 m, therewould be 12 rocks±8 S.D. within an observer's visible range. Incontrast, on slopes of 10° the mean outcropping rock density was 0.5rocks 1000 m−2±0.7 S.D, so given a conservative threshold detectionradius of 5 m, 0.04 rocks±0.05 S.D would be within visible range.Clearly, in areas of lower rock density there will be fewer potentialsites of naturally stimulated bioluminescence within the visible rangeof a stationary observer. The solid line in Fig. 4 shows the minimumdensity of protruding rocks required to ensure at least one potentialsite of natural bioluminescence within visible range as a function ofthe threshold detection radius.

The eyes of bathypelagic species are sophisticated andwell adaptedfor the detection of point sources of light (Warrant and Locket, 2004).The eye design of bathypelagic crustaceans enables high sensitivityat the expense of good spatial acuity. Such design would suit thedetection of stationary areas of increased bioluminescent activity.Based on these adaptations, Warrant and Locket (2004) speculatedthat bioluminescence must be an important sensory cue for bathype-lagic species, which our study supports. However, the cognition andinterpretation of bioluminescence by deep-sea fauna is not fullyunderstood and is likely to be highly species specific. Bioluminescencemay result in positive or negative phototactic responses (attracted to,or repelled by the light), or indifference from the observer. The use ofbioluminescent lures by deep water fish, cephalopods and siphono-phores (reviewed in Haddock et al., 2010) suggests that biolumines-cence serves as an attractant. Studies on net catches with and withoutthe addition of artificial light report a range of reactions from differentgroups and species including an increase in catch of some fish specieswith well developed visual systems (Gordon et al., 2002) and an

Fig. 4. Left y-axis: The number of protruding rocks within visual range of a stationaryobserver, as a function of the threshold detection radius, in an area with a rock densityof 145±97 rocks 1000 m−2 (long dash line) and 0.5±0.7 rocks 1000 m−2 (short dashline) (± standard deviation: dotted line). Right y-axis: minimum density of protrudingrocks (1000 m−2) required to provide at least one potential site of naturalbioluminescence within visual range of a stationary observer, given threshold detectionranges from 0 to 100 m (solid line).

567J. Craig et al. / Journal of Marine Systems 88 (2011) 563–567

increase in the number of cephalopods caught (Clarke and Pascoe,1998). Although this is not universally true, for example, Heger et al.(2007) reported a reduction in the number of deep sea eels enteringthe field of view of a camera as the intensity of bioluminescenceincreased during a baited experiment. In general, the reactions ofdecapods and other crustaceans to illuminated nets showed lower andunchanged catches (Hargreaves and Herring, 1992). Yet examples canalso be found where bioluminescence functions as a visual cue, e.g. forfeeding copepods (Nishida et al., 2002). Reactions among deep-seafauna are diverse and will also depend on the intensity and kinetics ofthe bioluminescent signal. Nonetheless it is reasonable to concludethat the presence of bioluminescence has the potential to influence thebehaviour of deep-sea fauna. As such, a localised increase in the rate ofbioluminescent events in the vicinity of specific sea floor featurescould spatially concentrate those behaviours, also concentrating anyindirect effects. For example, an increase in the density of mobilepredators could lead to a localisation of predation, competition forprey, or create a localised increase in organic faecal matter.

In this study we suggest that areas of rough terrain produce asubstantial increase in naturally occurring bioluminescence. Theability of many species to take advantage of this bioluminescenceindicates that it has the potential to influence their behaviour.

5. Conclusion

This is the first study to make observations of high bioluminescentactivity in an undisturbed habitat in the deep sea. It is unlikely to be arare event and we suggest rocky outcrops serve as a natural stimulusto the production of light in the deep sea. We suggest that the visualenvironment may be as varied as, and indeed correlated to, thephysical benthic habitat. Furthermore, the efficiency and capacity inwhich light is emitted and detected by most deep-sea organismssuggest that localised elevated bioluminescent activity could be asecologically significant as the physical environment itself. Thereforewe present these preliminary observations in the hope that othersubmersible operators will take the opportunity to make passive low-light observations to characterise the visual as well as physical deep-sea environment.

Acknowledgements

We thank the captain, crew and company of the RRS James Cook,cruises JC037 and JC048 and the ISIS ROV team at the NationalOceanography Centre, Southampton, UK. This work was supported bythe NERC Consortium Grant ECOMAR (Ecosystem of the Mid-AtlanticRidge at the SubPolar Front and Charlie Gibbs Fracture Zone (Grantno. NE/C512961/1). J. Craig was funded by UK NERC studentship (NE/F012020/1).

References

Aguilar, J., The ANTARES Collaboration, 2006. First results of the instrumentation linefor the deep-sea ANTARES neutrino telescope. Astropart. Phys. 26 (4–5), 314–324.

Amram, P., The ANTARES Collaboration, 2000. Background light in potential sites for theANTARES undersea neutrino telescope. Astropart. Phys. 13 (2–3), 127–136.

Bailey, D., Priede, I.G., 2002. Predicting fish behaviour in response to abyssal food falls.Mar. Biol. 141 (5), 831–840.

Clarke, G.L., Hubbard, C.J., 1959. Quantitative records of luminescent flashing of oceanicanimals at great depths. Limnol. Oceanogr. 4, 163–180.

Clarke, G.L., Kelly, M.G., 1965. Measurements of diurnal changes in bioluminescencefrom the sea surface to 2000 meters using a new photometric device. Limnol.Oceanogr. 10, R54–R66.

Clarke, M.R., Pascoe, P.L., 1998. The influence of an electric light on the capture ofoceanic cephalopods by a midwater trawl. J. Mar. Biol. Assoc. U. K. 78, 561–575.

Craig, J., Jamieson, A.J., Bagley, P.M., Priede, I.G., 2011. Seasonal variation of deep-seabioluminescence in the Ionian Sea. Nucl. Instrum. Meth. Phys. Res. A 626-627 (S1),S115–S117.

Craig, J., Jamieson, A.J., Heger, A., Priede, I.G., 2009. Distribution of bioluminescentorganisms in the Mediterranean Sea and predicted effects on a deep-sea neutrinotelescope. Nucl. Instrum. Meth. Phys. Res. A 602 (1), 224–226.

Craig, J., Jamieson, A.J., Hutson, R., Zuur, A.F., Priede, I.G., 2010. Factors influencing theabundance of deep pelagic bioluminescent zooplankton in the Mediterranean Sea.Deep Sea Res. Part I. 57 (11), 1474–1484.

Gillibrand, E.J.V., Jamieson, A.J., Bagley, P.M., Zuur, A.F., Priede, I.G., 2007a. Seasonaldevelopment of a deep pelagic bioluminescent layer in the temperate NE AtlanticOcean. Mar. Ecol. Prog. Ser. 341, 37–44.

Gillibrand, E.J.V., Jamieson, A.J., Bagley, P.M., Zuur, A.F., Priede, I.G., 2007b. Deep sea benthicbioluminescence at artificial food falls, 1,000–4,800 m depth, in the PorcupineSeabight and Abyssal Plain, North East Atlantic Ocean. Mar. Biol. 150 (6), 1053–1060.

Gordon, J.D.M., Bergstad, O.A., Pascoe, P.L., 2002. The influence of artificial light on thecaptureof deep-waterdemersalfishbybottomtrawling. J.Mar.Biol. Assoc.U.K. 82, 1–6.

Haddock, S.H.D., Case, J.F., 1994. A bioluminescent chaetognath. Nature 367 (6460),225–226.

Haddock, S.H.D., Case, J.F., 1999. Bioluminescence spectra of shallow and deep-seagelatinous zooplankton: ctenophores, medusae and siphonophores. Mar. Biol. 133(3), 571–582.

Haddock, S.H.D., Dunn, C.W., Pugh, P.R., Schnitzler, C.E., 2005. Bioluminescent and red-fluorescent lures in a deep-sea siphonophore. Science 309 (5732), 263.

Haddock, S.H.D., Moline, M.A., Case, J.F., 2010. Bioluminescence in the sea. Annu. Rev.Mar. Sci. 2, 443–493.

Hargreaves, P.M., Herring, P.J., 1992. The response of decapod and mysid crustaceans toartificially lighted trawls. J. Mar. Biol. Assoc. U. K. 72, 621–631.

Hartline, D.K., Buskey, E.J., Lenz, P.H., 1999. Rapid jumps and bioluminescence elicitedby controlled hydrodynamic stimuli in a mesopelagic copepod, Pleuromammaxiphias. Biol. Bull. 197, 132–143.

Heger, A., King, N.J., Morris, K.J., Bagley, P.M., Priede, I.G., 2008. Deep-sea pelagicbioluminescence over theMid-Atlantic Ridge. Deep Sea Res. Part II 55 (1–2), 126–136.

Heger, A., King, N.J., Wigham, B.D., Jamieson, A.J., Bagley, P.M., Priede, I.G., Pfannkuche,O., 2007. Bioluminescent aggregations of Vargula norvegica (Ostracoda) at artificialfood falls at 1000 m depth in carbonate mound provinces of the NE Atlantic. Mar.Biol. 151 (4), 1471–1478.

Herren, C.M., Haddock, S.H.D., Johnson, C., Orrico, C.M., Moline, M.A., Case, J.F., 2005. Amulti-platform bathyphotometer for fine-scale, coastal bioluminescence research.Limnol. Oceanogr. Methods 3, 247–262.

Klages, M., Muyakshin, S., Soltwedel, T., Arntz,W.E., 2002. Mechanoreception, a possiblemechanism for food fall detection in deep-sea scavengers. Deep Sea Res. Part I 49(1), 143–155.

Lokkeborg, S., Olla, B.L., Pearson, W.H., Davis, M.W., 1995. Behavioural responses ofsablefish, Anoplopoma fimbria, to bait odour. J. Fish Biol. 46, 142–155.

Meyer, D.L., 1982. Food and feeding mechanisms: Crinozoa. In: Jangoux, M., Lawrence, J.M. (Eds.), Echinoderm Nutrition. CRC Press, Rotterdam, pp. 25–42.

Nishida, S., Ohtsuka, S., Parker, A., 2002. Functional morphology and food habits ofdeep-sea copepods of the genus Cephalophanes (Calanoida: Phaennidae):perception of bioluminescence as a strategy for food detection. Mar. Ecol. Prog.Ser. 227, 157–171.

Piontkovski, S.A., Tokarev, Y.N., Bytukov, E.P., Williams, R., Kiefer, D.A., 1997. Thebioluminescent field of the Atlantic Ocean. Mar. Ecol. Prog. Ser. 156, 33–41.

Priede, I.G., Bagley, P.M., Way, S., Herring, P.J., Partridge, J.C., 2006. Bioluminescence inthe deep sea: free-fall lander observations in the Atlantic Ocean off Cape Verde.Deep Sea Res. Part I. 53 (7), 1272–1283.

Priede, I.G., Jamieson, A., Heger, A., Craig, J., Zuur, A.F., 2008. The potential influence ofbioluminescence from marine animals on a deep-sea underwater neutrinotelescope array in the Mediterranean Sea. Deep Sea Res. Part I. 55 (11), 1474–1483.

Rivers, T.J., Morin, J.G., 2008. Complex sexual courtship displays by luminescent malemarine ostracods. J. Exp. Biol. 211, 2252–2262.

Robison, B.H., Reisenbichler, K.R., Hunt, J.C., Haddock, S.H.D., 2003. Light production by thearmtipsof thedeep-seacephalopodVampyroteuthis infernalis. Biol. Bull. 205, 102–109.

Sainte-Marie, B., Hargrave, B.T., 1987. Estimation of scavenger abundance and distanceof attraction to bait. Mar. Biol. 94, 431–443.

Turner, J.R., White, E.M., Collins, M.A., Partridge, J.C., Douglas, R.H., 2009. Vision inlanternfish (Myctophidae): adaptations for viewing bioluminescence in the deep-sea. Deep Sea Res. Part I. 56 (6), 1003–1017.

Warrant, E.J., Locket, N.A., 2004. Vision in the deep sea. Biol. Rev. 79 (3), 671–712.Widder, E., 2002. Bioluminescence and the pelagic visual environment. Mar.

Freshwater Behav. Physiol. 35, 1–26.Widder, E.A., Bernstein, S.A., Bracher, D.F., Case, J.F., Reisenbichler, K.R., Torres, J.J.,

Robison, B.H., 1989. Bioluminescence in the Monterey Submarine Canyon: imageanalysis of video recordings from amidwater submersible. Mar. Biol. 100, 541–551.

Widder, E.A., Frey, C.L., Borne, L.J., 2003. HIDEX Generation II: a new and improvedinstrument for measuring marine bioluminescence: OCEANS 2003. Proceedings,2214, pp. 2214–2221.

Widder, E.A., Robison, B.H., Reisenbichler, K.R., Haddock, S.H.D., 2005. Using red light forin situ observations of deep-sea fishes. Deep Sea Res. Part I 52 (11), 2077–2085.

Wilson, R.R., Smith, K.L., 1984. Effect of near-bottom currents on detection of bait by theabyssal grenadier fishes, Coryphaenoides spp. recorded in situ with a video cameraon a free vehicle. Mar. Biol. 84, 83–91.

Woodland, D.J., Cabanban, A.S., Taylor, V.M., Taylor, R.J., 2002. A synchronized rhythmicflashing light display by schooling Leiognathus splendens (Leiognathidae: Perci-formes). Mar. Freshwater Res. 53, 159–162.