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Journal for Nature Conservation 19 (2011) 363– 367

Contents lists available at ScienceDirect

Journal for Nature Conservation

jou rn al h omepage: www.elsev ier .de / jnc

hort communication

ostural instability and akinesia in a pantropical spotted dolphin, Stenellattenuata, in proximity to operating airguns of a geophysical seismic vessel

oward Graya,∗, Koen Van Waerebeekb

School of Biological and Biomedical Sciences, University of Durham, South Road, DH1 3LE, UKCetacean Conservation Medicine Group, Centro Peruano de Estudios Cetológicos (CEPEC), Museo de Delfines, Lima 20, Peru

r t i c l e i n f o

rticle history:eceived 9 February 2011eceived in revised form 4 May 2011ccepted 23 June 2011

eywords:coustic distress

a b s t r a c t

Aberrant behaviour including erratic locomotion was observed in a pantropical spotted dolphin 600 mahead of an airgun array during 3D seismic explorations off Liberia in March 2009. The dolphin, presum-ably in acoustic distress, lifted its head and cervical region above the surface in an oblique, strikingly rigidposture during 5 min. Turbulent white-water evidenced a major propulsory thrust. Incremental posturalinstability and apparent exhaustion progressed to a catatonic-like state of akinesia as the dolphin rolledover onto one side, then its back before sinking virtually motionless close to the airgun array. Unless itrecovered full locomotory control, asphyxiation was inevitable. Potential internal injury is discussed, both

ehaviouratatonia

njuryiberiayopathy

tress

acoustic-mediated and from extreme exertion (exertional myopathy, rhabdomyolysis and myoglobin-uric nephrosis). As behaviour was spatially and temporally closely associated with firing seismic airguns,we suggest a cause–effect relationship. Differential diagnoses of pre-existing morbidity, senescence, orintoxication are considered possible but unlikely.

© 2011 Elsevier GmbH. All rights reserved.

eismic survey

ntroduction

The negative effects of anthropogenic noise on cetaceans areenerally well-documented (e.g. Gordon et al. 2003; Nowacek et al.007; Stone 2003; Weilgart 2007) and include avoidance behaviourGoold 1996; Richardson et al. 1995; Stone 2003; Weir 2008),ehavioural changes (Bowles et al. 1994; Southall et al., 2007),tress (Bateson 2007; Romano et al. 2004), migration route shiftsRichardson et al. 1999), physiological or auditory damage (Gordont al. 2003; Ketten et al. 1993) and mortality (Fernández et al. 2004,005; Jepson et al. 2003) amongst others.

As highest acoustic energy levels by seismic exploration areroduced at low frequencies of 10–200 Hz and overlap with mys-icete signal frequencies of 16–500 Hz (reviewed in Weir 2008),

ysticetes are thought to be more sensitive to seismic activi-ies than odontocetes (Nowacek et al. 2007; Richardson et al.995; Richardson & Würsig 1997). However, Goold and Fish (1998)howed that incidental noise emissions during seismic surveysominate the bandwidth within odontocete auditory range (200 Hz

o 22 kHz) at distances of up to 2 km or more from the airgun source.lthough behavioural effects of airgun sound on small odonto-etes have been poorly studied (Weir 2008), dolphins observed

∗ Corresponding author.E-mail address: howard gray@btinternet.com (H. Gray).

617-1381/$ – see front matter © 2011 Elsevier GmbH. All rights reserved.oi:10.1016/j.jnc.2011.06.005

from seismic vessels in operation are regularly seen moving awayfrom the acoustic source (Bain & Williams 2006; Calambokidis &Osmek 1998; Stone 2003; Stone & Tasker 2006; Weir 2008; authors,personal observations). Encounter rates for several small odonto-cetes off the UK were significantly lower and distance to sightingswas significantly higher during periods when air-guns were firing(Stone 2003). Goold (1996) suggested that within 1 km short-beaked common dolphins, Delphinus delphis, found the signalsfrom a seismic source aversive. Striking short-term, short-rangeresponses were reported for Atlantic spotted dolphins Stenellafrontalis off Angola (Weir 2008). Groups occurred at a signifi-cantly greater distance from the airgun array (p < 0.001) duringfull-array operations than during guns-off periods, while positive-approach behaviour (N = 9) occurred only during guns-off periods(Weir 2008).

Case study

On 18 March 2009, an adult-sized pantropical spotted dolphin,Stenella attenuata (Gray, 1846) was closely observed during 3Dseismic explorations by R/V GeoBarents between ca. 15–50 nm off-

shore Monrovia, Liberia from 27 February to 4 May 2009. The singledolphin of sighting HG-037 displayed aberrant behaviour, the cir-cumstances of which are discussed below in an effort to elucidatethe potential cause.

364 H. Gray, K. Van Waerebeek / Journal for Nature Conservation 19 (2011) 363– 367

Fig. 1. Observation track log and location of cetacean sightings on 18 March 2009 off Liberia. HG-036, 08:06 h, 200 unidentified Delphinidae at N06.05122◦ , W010.90085◦ ,airguns firing. HG-037, 13:31 h, 1 Stenella attenuata at N06.00240◦ , W010.94498◦ , airguns firing. HG-038, 13:52 h, 300 unidentified Delphinidae at N06.01798◦ , W010.96295◦;airguns firing. HG-039, 17:01 h, 7 Globicephala macrorhynchus at N06.14442◦ , W011.11383◦ , airguns inactive. HG-040, 17:02 h, 200 unidentified Delphinidae at N06.1499◦ ,W011.11675◦ , airguns inactive.

Table 1Record of operations.

Line Time soft start began Time of full power Time of start of line Time of end of line Time airguns stopped

Line 1 01:50 02:10 02:36 05:06 05:06Line 2 07:21 07:41 08:06 08:47 08:47Line 3 12:24 12:44 13:07 15:38 15:38Line 4 17:21 17:41 18:05 20:24 20:24

G-037

oiwldwa1oc(d

i

Fig. 2. Observed movement (dotted line) of pantropical spotted dolphin H

During 601 min on watch on 18th March, HG made five sightingsf delphinids. The observation track-log, with sighting locations,s plotted in Fig. 1. The distance between adjacent survey lines

as approximately 8800 m. In the course of the day, four ‘infill’ines1 were run (Table 1). A 30-min pre-shoot watch was con-ucted before every ‘soft start’ in daylight hours. Observer heightas 11.80 m at the time of observation. The soft start was initi-

ted more than 1 h before dolphin HG-037 was encountered at3:31 h, position N06.00240◦, W010.94498◦, approximately 19 nmff the Liberian coast where water depth was 520 m. Fair weather

onditions included a Beaufort sea state 3 and good visibility>3 km). The vessel was traveling at approximately 4.0 kts and theeployed Sondera G-airguns in towed array (Fig. 2) were operat-

1 New tracklines designed for a second attempt at surveying in an area that wasncompletely surveyed during a first pass-over, often due to some technical problem.

relative to the port side of the vessel with layout of towed seismic array.

ing at full power during the observation. Their main specificationswere: 2 × 3400 in.3 volume; air pressure 2000 psi; shot interval25 m flip-flop (i.e. 50 m per source); source depth 6 m (±1.0 m)and source separation 50 m; peak–peak 166.4 bar m; P/b ratio min-imum 29.5:1; maximum timing error ±1 ms. While no specificlegislation exists in Liberia regulating mitigation of marine mam-mal disturbance during seismic surveys, the UK’s Joint NatureConservation Committee (JNCC) guidelines were followed (seewww.jncc.gov.uk). JNCC does not require active measures after softstarts, the industry’s standard gradual power ramping-up proce-dure, from minimal to full-power over a 20 min period, designed toallow marine mammals sufficient time to move away.

The initial sighting cue at 13:31 h consisted of dolphin HG-037

moving erratically at the surface, approximately 600 m ahead of theairgun array. Both initial posture and locomotion differed from anydolphin behaviour known to the authors. This individual slowlymoved forward, non-directionally, while lifting its anterior body

H. Gray, K. Van Waerebeek / Journal for Nature Conservation 19 (2011) 363– 367 365

Fig. 3. Pantropical spotted dolphin HG-037 moving erratically with a sustained head-out posture a few hundred meters from an active seismic array, (A) facing away fromt cating

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he vessel, and (B) producing considerable white-water turbulence in its wake indi

n an oblique, strikingly rigid, head-up position, in stark contrastith the normal undulatory movements of delphinids. As evi-enced by turbulent white-water in its wake, the dolphin produced

major propulsory thrust while attempting, initially successfully,o keep head and cervical region above the water surface (Fig. 3).his behaviour lasted for ca. 5 min when the dolphin increasinglytruggled to maintain posture to keep head and cervical regionbove the surface (Fig. 3). Eventually it slid into a catatonic-liketate of akinesia and postural instability as it, apparently passively,olled over onto one side, then onto its back, exposing ventrum andail. The dolphin was last seen sinking with minimal movements,ome 300 m ahead of the airgun array, and merely 200 m from thebserver (closest distance). As the vessel continued its course, thenimal would have found itself within an estimated 100 m radiusrom the nearest airgun if it did not move from where it was lastighted.

While potential morbidity or senescence cannot be ruled out,o external indicators of a pre-existing condition were observedespite the sustained surface behaviour allowing good views ofhe dolphin’s anterior body. Diseases like morbilliviral encephali-is, neurobrucellosis and cerebral toxoplasmosis affect the centralervous system and while little is known on their clinical manifes-ations in delphinids before they are found moribund or dead on aeach (Di Guardo et al. 2010; Domingo et al. 1995; Hernández-Morat al. 2008), erratic behaviour could occur. There were no signs ofmaciation, such as a post-occipital or dorso-lateral depression androtruding ribs, commonly associated with malnutrition or chronicisease. Neither was any cutaneous disease apparent, which fre-uently involve highly visible lesions on trunk and dorsal fin (e.g.an Bressem et al. 2007). Intoxication by phycotoxins produced by

harmful algal bloom (Van Dolah 2000) was extremely unlikely,oth because no algal blooms (red tides) were encountered in theurvey area despite intense observer effort and because Liberia’sropical waters lack significant populations of pelagic phytoplank-on feeders (e.g. anchovies, sardines, krill), abundant in majoroastal upwelling ecosystems, and necessary vectors to transfer

hycotoxins to upper trophic level predators (Bargu et al. 2002),

ncluding delphinids. No bleeding or other signs of external physi-al trauma were detected and a prior predator attack, intraspecificggression, or collision with a vessel, were also discarded as highly

major propulsive effort.

implausible. Finally, no parasitic fish such as cookie-cutter shark(Isistius brasiliensis) or suckerfish (Echeneididae) were present.

The auditory system is the primary sensory system in odonto-cete cetaceans (Herman & Tavolga 1980; Oelschläger & Oelschläger2002; Popper 1980; Slijper 1979), and although debate is still ongo-ing about the main channels of sound reception in delphinids,leading hypotheses point to the rostrum, auditory meatus or theentire head (Popov et al. 2008; Popper 1980). A parsimoniousexplanation then for the aberrant behaviour could be that the dol-phin suffered severe acoustic distress, if not internal injury, andattempted to lift its anterior body above the surface in an effortto shield its sensitive rostrum, auditory meatus, tympano-perioticcomplex and paranasal air sacks from water-borne high-amplitudeacoustic energy.

The observed erratic locomotion was essentially dissimilar from‘spy-hopping’ behaviour during which a cetacean raises its headvertically above the surface and remains either motionless in thatposition or rotates on its longitudinal axis, but does not movearound. Spy-hopping orients the cetacean (but not reported in S.attenuata) to nearby or distant surface features through a visualinspection of surroundings, while it may have social functions aswell (Madsen & Herman 1980; Williams et al. 2002). The animal’sorientation away from the vessel for part of the time (Fig. 3) wasinconsistent with spy-hopping, as the vessel represented the onlydiscernible seascape feature.

In their review of behavioural and physiological responses ofcetaceans to anthropogenic sound, Southall et al. (2007) pro-vided further potential clues. Extreme sound exposure may elicita vestibular response leading to behavioural change or stress-induced hemorrhagic diatesis. Physiological changes to pulmonary,cardiac and other functions may potentially lead to tissue damagein extreme cases. Internal injury can also occur through acousticresonance of tissues or acoustic-mediated bubble formation andexpansion (Fernández et al. 2005; Southall et al. 2007). In humans,acute trauma to the vestibular system (semicircular canals andvestibular nuclei) can lead to sudden vertigo, impairing the ability

to maintain posture and balance (Konrad 1990). Head trauma maycause catatonic stupor that reduces motor activity to zero (Olendorfet al. 2006). Extrapyramidal rigidity and catatonia can both be man-ifestations of brain-stem involvement (Shephard & Wadia 1956)

3 or Nat

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66 H. Gray, K. Van Waerebeek / Journal f

hile cerebral oedema has long been known associated with casesf catatonia (Greenfield 1939). Any of these conditions would beongruent with the progressive deterioration of locomotive ability,oss of equilibrium and catatonic-like akinesia observed in HG-037.lthough ‘passive-sinking’ has been reported in pantropical spot-

ed dolphins and spinner dolphins Stenella longirostris trapped (notntangled) in tuna purse-seine nets in the eastern tropical PacificCoe & Suntz 1980; Curry, 1999; Oliveros & Maldonado 2002),nder those circumstances sinking behaviour was mainly tran-ient and deemed physiological. Nonetheless, dolphins that died inurse-seine nets often showed fatal heart damage possibly relatedo elevated stress-hormones including catecholamines (Edwards007). Stress and exertion are also well-documented causes ofhabdomyolysis and myoglobinuric nephrosis (Herráez et al. 2007).

Although no significant statistical difference was foundMann–Whitney U = 13, p = 0.55, n = 9) between estimated dis-ances (in m) at first sighting of S. attenuata groups during firingmean = 1575, SD = 1417, n = 4) vs. non-firing guns (mean = 820,D = 597, n = 5), sample sizes were very small. We observedantropical spotted dolphins (n = 9) consistently avoiding the ves-el when airguns were firing. The dolphins would move away,ften at great speed, even when at several kilometers distancerom the vessel (maximum distance ca. 3500 m). For instance, dur-ng a pre-shoot search on 29 January 2009 at 16:50 h with a softtart procedure due to be initiated, KVW detected an estimated 90antropical spotted dolphins on the track-line ca. 2000 m aheadf the vessel (sighting KVW-008). Although the dolphins were out-ide the pre-defined 500 m safety perimeter they were approachingapidly in a course headed straight to the bow, with apparent intento bow-ride. The Navigation Unit decided to immediately fire twomall (948.8 cm3/60 in.3) airguns as ‘warning shots’ in the hope theolphins would abort their approach. KVW visually monitored theroup through 7 × 50 mm binoculars while in continuous radio con-act with the acting Navigator. The controlled action was instantlyuccessful as the dolphins stopped, turned and then moved awayrom the vessel at the surface, porpoising at high speed, just secondsfter firing the small airguns.

Atypically, dolphin HG-037 was seen alone, in contrast withther S. attenuata groups off Liberia comprising between 7 and00 individuals (personal observations, unpublished data, n = 9)nd the species’ known gregarious nature (Jefferson et al. 2008;errin 2001, 2009). However, it was unclear how, and when, thenimal became separated from its group. Separation may have beenrief, even momentaneous, and other members of a small groupould have evaded detection while the aberrant-behaving dolphinalled all the attention from the single observer. The individualay have belonged to a group of unidentified delphinids (HG-036)

ighted 5 h 25′ earlier which was thought to have been ‘frightened’way in SE direction during infill shooting and may have been re-ncountered at 13:52 h while running infill lines heading NW theame day (Fig. 1).

onclusion

Pantropical spotted dolphin HG-037 did not move away fromn approaching, active seismic gun array, but instead resorted ton evasive posture. Apparent physical exhaustion, possibly com-ounded by internal acoustic injury, within minutes ushered intohe observed postural instability, akinesia and sinking. Asphyxi-tion and death likely ensued, unless it regained full locomotoryontrol. Alternatively, excessive muscular exertion may have led

o exertional myopathy, myocardial lesions, acute rhabdomyoly-is and associated myoglobinuric nephrosis (Herráez et al. 2007;

illiams & Thorne 1996). As the documented behaviour was spa-ially and temporally closely associated with seismic airguns firing

ure Conservation 19 (2011) 363– 367

at full power, we believe a cause–effect relationship may haveexisted. We suggest that under certain circumstances, includ-ing short range, the impact of seismic acoustic surveying on thehealth and survival of individual dolphins may be deleterious,adding weight to the recommendation for a strictly precautionaryapproach to management and regulation (Gordon et al. 2003) andthe compelling need for focused behavioural research.

Acknowledgements

Robert Baldwin and Dr. Marie-Francoise Van Bressem arewarmly thanked for constructive comments on an earliermanuscript. Two anonymous reviewers also contributed with valu-able remarks.

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