Investigation of the common dolphin mass...

Investigation of the common dolphin mass stranding event in Cornwall, 9th June 2008

(Funded under a variation to contract number CR0364)

© PA photos

Compiled by P.D. Jepson and R. Deaville (ZSL)

Contributing Authors- K. Acevedo-Whitehouse (ZSL), J. Barnett (VLA), R.L. Brownell (SFSC), A. Colloff (VLA), F. C. Clare (ZSL), N. Davison (VLA), R. Law (CEFAS), J. Loveridge (CWTMSN), S.K. Macgregor (ZSL), S. Morris (CEFAS), R. Penrose (MEM), M. Perkins (ZSL), E. Pinn (JNCC), V. Simpson (WVIC), M. Tasker (JNCC), N. Tregenza (CWTMSN), A.A. Cunningham (ZSL) and A. Fernández (ULPGC)

This report results from work conducted by the collaborative UK Cetacean Strandings Investigation Programme. Partner organisations are Institute of Zoology, Zoological Society of London (ZSL), the Scottish Agricultural College, Inverness (SAC),

the Natural History Museum (NHM) and Marine Environmental Monitoring (MEM).

Other organisations that contributed to this report include British Divers Marine Life Rescue (BDMLR), Centre for Environment, Fisheries and Aquaculture Science (CEFAS), Cornwall Wildlife Trust Marine Strandings Network (CWTMSN), Joint Nature Conservation Committee (JNCC), Southwest Fisheries Science Centre (SFSC), Universidad de las Gran Palmas Gran Canaria (ULPGC), Veterinary

Laboratory Agency, Truro (VLA) and Wildlife Veterinary Investigation Centre in Cornwall (WVIC).

Executive summary Cetacean mass stranding events (MSEs) have puzzled humans for centuries. On the morning of 9 June 2008 common dolphins (Delphinus delphis) were found, some swimming, some stranded and some dead, in and around a small tidal tributary (Porth Creek, Percuil River) of the Fal Estuary in Cornwall, in the southwest of England. The first report of the MSE was received by Falmouth Coastguard at 08:21hrs reporting a single dolphin stranded in Porth Creek. Several groups of dolphins were subsequently seen very close to shore and exhibited “milling” and other agitated behaviours. At least one large group of 40-60 common dolphins had been seen unusually close to shore in the Falmouth Bay region on 5, 7 and 8 June and may have been the group that subsequently stranded. Common dolphins are frequently seen in Falmouth Bay, but rarely so close to shore or within the estuary. Twenty-six dolphins died (all carcasses were found in fresh condition on 9 June) and a similar or larger number were refloated/herded back to sea by rescuers. This is only the fourth UK common dolphin mass stranding since systematic recording of strandings began in 1913 and the first in this locality. The UK Government (Defra) promptly funded a variation of the current UKCSIP contract for the Institute of Zoology (Zoological Society of London) to lead a collaborative and wide-scale investigation into the MSE and to try to identify the specific cause. The investigation included detailed pathological examinations and a range of additional diagnostic tests (including microbiology, histopathology, morbillivirus infection and analyses for algal and chemical toxins), all using internationally standardised methodologies. Interviews with rescuers, local maritime and other agencies have been conducted for potential trigger factors of the MSE. On post-mortem examination, all 26 dead dolphins were in good nutritive status and had empty stomachs. There was no evidence of significant infectious disease or acute physical injury. Tissue samples from the seven adult dolphins were free of harmful algal toxins and the levels of organochlorines (polychlorinated biphenyls and pesticides such as DDT), trace metals and butyltins were at lower levels than recorded in stranded common dolphins in south-west England in 1990-92. The auditory apparatus (ears) were grossly normal in all cases. Detailed histological examinations of ears are ongoing but, due to mild decomposition in all cases, are unlikely to provide further insight. No witness to the entry of the dolphins into the estuary has been found but the local tidal regime and the timing of agitated behaviours seen in other groups of near-shore common dolphins suggests that the likely entry of the dolphins into Porth Creek was most probably sometime after 06:30-07:00hrs on 9 June, although the dolphins could also have entered the inner parts of Porth Creek earlier on 9 June. Climatic conditions were normal and there were no reports from local fisheries of unusual fish distribution and no records of unusual commercial shipping or seismic surveys. A number of potential causes of this MSE can be either excluded or considered highly unlikely. These include distemper (morbillivirus), brucellosis, other infectious diseases, fat embolism, gas embolism (decompression sickness), boat strike, by-catch, attack from killer whales (Orcinus orca) or bottlenose dolphins (Tursiops truncatus), feeding unusually close to shore immediately before the MSE, ingestion of harmful chemical or algal toxins, abnormal weather/climatic conditions and high-intensity acoustic inputs from seismic airgun arrays and natural sources (e.g. earthquakes).

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An international naval exercise was conducted in the South Coast Exercise Area prior to the MSE. Information provided by the UK Ministry of Defence, under legally-binding Freedom of Information legislation, indicates a period of approximately 60 hours between the cessation of mid-frequency (1-10kHz) antisubmarine sonar deployment and the discovery of the MSE. Mid-frequency sonars were therefore considered too temporally remote to have directly triggered the MSE. A helicopter flying exercise was scheduled for 08:00-13:30hrs on the morning of 9 June in Falmouth Bay (North), Falmouth Bay and Mounts Bay regions but the first flight to leave RNAS Culdrose was at 08:58hrs on 9 June (37 minutes after the MSE was first reported) and the first incoming flight landed at 09:17hrs and this flight did not transit Falmouth Bay. The recorded naval helicopter flights into/out of RNAS Culdrose therefore cannot have initially triggered the MSE. However, naval helicopter activity, or some other unknown factor(s), may have caused the apparently agitated/flight response in the group of dolphins later seen entering the inner part of Falmouth Harbour around 09:30hrs (approx 80-90mins after the initial discovery of the MSE), although detailed flight records were not available at the time to fully explore this consideration further. The large dolphin group(s) seen unusually close to shore in the days prior to the MSE may have been at increased risk of stranding and subsequently stranded en masse. The reason for this near-shore distribution is not known but natural (e.g. foraging closer to shore), anthropogenic (e.g. naval activities leading up to 9 June) or other unknown factor(s) could have played a contributory role. The MSE findings were most consistent with an adverse group behavioural response to a specific trigger(s) within an otherwise healthy social group of common dolphins on the morning of 9 June. Alternatively, the stranding mechanism itself could have involved an intrinsic “error of navigation” or a confluence of other unknown factors (anthropogenic and/or natural). Ultimately, in conclusion, a definitive cause of the MSE could not be identified. Greater insight into the causes of any future MSEs may require either a direct observation of the onset, or the emergence of an unusual level of coincidence of MSEs or violent reactions with one or more causal factors.

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Contents

Executive Summary 2 Contents 4 1 List of Figures and Tables 5 2 Background 6 3 Introduction 6 4 Methods 9 5 Results 13 6 Discussion 20 7 Conclusions 24 8 Recommendations 25 9 References 26 10 Glossary of terms and acronyms 29 11 Acknowledgments 30

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1 List of figures and tables Figures Figure 1 Known sites of live and dead common dolphins in Falmouth Bay, Cornwall, 8 9

th-11

th June 2008 (inset map shows location of Falmouth in UK)-

courtesy of CWT Marine Strandings Network Figure 2 Known sites of live and dead common dolphins in Porth Creek, Percuil 8 River, Cornwall, June 9

th 2008 (shows area within red box in Figure 1)-

courtesy of CWT Marine Strandings Network Figure 3 All common dolphin strandings (live and dead) in Cornwall (by day) 13 in Jan-Dec 2008. (Data: CWTMSN). Figure 4 Mean summed 25CBs levels in UK-stranded adult female common dolphins 15 from 1990-1992 (n=8) and from the MSE in 2008 (n=6) Figure 5 Distribution of high-intensity acoustic activities nearest to stranding location 18 Figure 6 Temporal distribution (5-9 June) of naval acoustic activities and possible 19 bottlenose dolphin sighting in western part of South Coast Exercise Area

Tables Table 1 Live sightings of common (D. delphis) and bottlenose dolphins 12 (T. truncatus) in or near Falmouth Bay, Cornwall (5-9 June 2008) Table 2 Pathological data and diagnostic test results on 26 common dolphins 16 examined at necropsy

Plates Front Dead common dolphins at Porth Creek in Cornwall, June 9

th 2008 Front

page © PA photos page Plate 1 Dead common dolphins awaiting necropsy by the CSIP at Porth creek 9 in Cornwall, June 9

th 2008 (image copyright ZSL)

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2 Background The UK Cetacean Strandings Investigation Programme (CSIP) has been in operation since 1990 and is currently funded by Defra and the Devolved Administrations. It coordinates the investigation of all whales, dolphins and porpoises (collectively known as cetaceans), marine turtles and basking sharks that strand around the UK coastline each year. As well as documenting each individual stranding, a proportion of all strandings are retrieved for investigation at post-mortem to allow a cause of death to be established where possible. The data and samples collected during the course of research have also facilitated a large number of international collaborations, which have addressed a wide range of scientific questions. Further information and background to the CSIP may be found at www.ukstrandings.org.

3 Introduction Mass stranding events (MSEs) are commonly described as two or more cetaceans (excluding a cow-calf pair) of the same species coming ashore, usually alive, at the same time and place (Geraci and Lounsbury 2005). Historically, at least 19 cetacean species have been affected, with some species, including false killer whales (Pseudorca crassidens), long-finned pilot whales (Globicephala melas), short-finned pilot whales (Globicephala macrorhynchus), Atlantic white-sided dolphins (Lagenorhynchus acutus) and white beaked dolphins (Lagenorhynchus albirostris), stranding at higher frequencies than others (Odell 1987; Geraci and Lounsbury 2005). The cause of these strandings has puzzled humans for centuries and, although numerous theories have been developed, few MSEs have been studied in detail and seldom has a definitive cause been established (reviewed in Geraci and Lounsbury 2005). Cetaceans that mass strand are generally pelagic odontocetes with a highly evolved social structure (reviewed in Geraci and Lounsbury 2005). Proposed causal factors for cetacean MSEs are numerous and include: becoming trapped on a receding tide (e.g. in long meandering channels, broad tidal flats, strong or unusual currents, extreme tidal flow or volume); navigational errors associated with topographical features forming natural “whale traps” (such as Wellfleet Bay, Cape Cod, Massachusetts, USA) (Wiley et al 2001); geomagnetic disturbances and errors in navigation while following geomagnetic contours; disturbance of echolocation by multiple reflections in bays (Sundarama et al 2006); pelagic cetaceans following prey close inshore; escaping from predators; disease in one or more individuals in a social group leading to some or all of the remainder of the group stranding; algal toxins and unusual environmental conditions such as electrical storms and other meteorological events; earthquakes and high-intensity acoustic fields (reviewed in Geraci and Lounsbury 2005). Species-specific behaviour in response to “panic” is also suggested as a potential factor explaining why some cetacean species mass strand more frequently than others (reviewed in Geraci and Lounsbury 2005). At 08:21hrs (BST) on 9 June 2008, the initial report was received by Falmouth Marine Coastguard Agency of a stranded common dolphin (Delphinus delphis) in Porth Creek, a small tributary of the Percuil River. Percuil River is a large tributary of the Fal Estuary, a deep tidal ria in Cornwall, in the southwest of the UK that has a tidal range of around 5m (see Figures 1 and 2). Subsequently, trained volunteers worked during the day on foot, in boats and swimming, to recover more carcasses

http://www.ukstrandings.org/

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and to try to herd larger groups of live common dolphins back out to sea. The total number of dolphins involved in the MSE is not definitely known, but 24 common dolphins were eventually found dead in Porth Creek on 9 June and another two that stranded alive (one in Porth Creek and one near Trelissick approx. 6.5km NNW of Porth Creek in the River Fal) were euthanized. All of the dead dolphins retrieved for necropsy in Porth Creek were found below the high water level. A dead dolphin was reported floating at the mouth of the Helford River on 11 June but this was not confirmed and no carcass was obtained for necropsy. The stranding locations on 9 June covered approximately 20 km of the Falmouth Bay and estuary coastline from Gillan Creek to Trelissick (Figures 1 and 2). Groups of free-swimming common dolphins were first reported to be seen at Porth Creek at 08:21hrs, Falmouth harbour at 09:30hrs and Gillan Creek at 16:30hrs on the same day (see Figures 1 and 2 and Table 1). Eyewitnesses consistently described their milling behaviour as “swimming continuously in tight circles, being vocal, fluke slapping, leaning sideways, and often with one or more individuals attempting to strand”. The dolphins in Falmouth harbour were also described as “appearing to ignore boats and the presence of humans and were resistant to attempts to herd them out of the harbour”. An unknown number of dolphins were successfully guided into the main estuary and swam towards con-specific(s) further out in deeper water. It is not known whether any of the dolphins that were seen free-swimming close to shore on the morning of 9 June at Place and Porth Creek were also any of those seen later that morning in Falmouth Harbour and that afternoon at Gillan Creek and Trelissick. High water in Porth Creek on 8 June was at 09:44 and 21:52 hrs and on 9 June at 10:37 hrs (BST). The dolphins furthest into the creek were at a point where the only water present at low tide is a shallow stream. The weather on the day of the MSE and on the days immediately prior to the event, was dry and sunny with no unusual storm activity in the region (data: UK Met Office). The objectives of the present study were to analyse the pathological findings from the individuals that stranded and died, and to investigate all available evidence to determine possible causes of the MSE.

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Figure 1 Known sites of live and dead common dolphins in Falmouth Bay, Cornwall, 9-11 June 2008 (inset map shows location of Falmouth in UK)- courtesy of CWT Marine Strandings Network

Figure 2 Known sites of live and dead common dolphins in Porth Creek, Percuil River, Cornwall, June 9 2008 (shows area within red box in Figure 1)- courtesy of CWT Marine Strandings Network

4 Methods The investigation involved two key components, the collection of background data on the location of animals (both live and dead) and of any activities in the area that may have played some role in the MSE, and secondly, conducting detailed necropsies (post-mortem investigations) on all dead animals and further analytical tests to investigate other potential factors for the MSE. This section provides detailed information on the methodology used in this investigation.

Plate 1 Dead common dolphins await necropsy at Porth Creek in Cornwall, June 9 2008 (image

copyright ZSL) Information on live and dead dolphins involved in the MSE Information on the times and locations of live and dead-stranded common dolphins involved in the MSE was gathered from a variety of opportunistic sources. Volunteers were interviewed about 2 weeks after the event and further information was solicited from bystanders and local maritime agencies including the Coastguard, the Falmouth Harbour Authority and the Cornwall Sea Fisheries Committee. Anecdotal reports from eyewitnesses of the events prior to, during and after the MSE were examined to try to clarify the timing and significance of any activities that may have had a bearing on the event. Collated information is shown in Figures 1 and 2 and Table 1.

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Gross necropsies Carcasses were recovered from the intertidal zone and all 26 dead common dolphins were systematically examined using a standard necropsy protocol (Jepson et al 2005; Jepson 2005). The carcass condition at necropsy was considered fresh (n=10), slightly decomposed (n=10) or moderately decomposed (n=6). Sexual maturity was estimated from body length and gonadal appearance. A standard set of tissue samples was taken, depending on carcass condition, for a range of standard diagnostic tests including histopathology, microbiology, parasitology, molecular detection of morbillivirus and other diagnostic studies. Bacteriology Tissue samples or swabs of selected tissues were taken aseptically for aerobic, anaerobic and capnophilic incubation bacteriological examination using standardised methods (Jepson et al 2005; Jepson 2005). Routine bacterial cultures of a range of tissue including liver, kidney, lung and brain were inoculated directly onto either Columbia blood agar base (Oxoid, CM331) with 5% horse blood and incubated aerobically, anaerobically or capnophilically at 37°C and observed at 1, 2 and 5 days, or inoculated onto 5% sheep blood agar (Oxoid, CM0271) and MacConkey agar (Oxoid CM0007) and incubated at 37°C in a capnophilic atmosphere and examined daily for 7 days. Lung samples were incubated aerobically on Columbia blood agar base (Oxoid, CM331) with 5% horse blood and Sabourauds dextrose agar (Oxoid CM41) in an aerobic atmosphere for fungal isolates. Any organisms recovered were identified using conventional methods including growth characteristics, colony morphology, staining properties and biochemical characterisation using the API identification system (bioMérieux, France). Culture methods and identification of Brucella species isolated from tissues utilised standardised methodologies similar to Foster et al. (2002) and confirmed as Brucella ceti by PCR amplification of an IS711 element downstream of the base-pair (bp) 26 gene and PCR amplification of the outer membrane proteins (omp) 2 locus and restriction with a selection of enzymes (Cloeckaert et al 2000; Cloeckaert et al 2001). Histopathology A range of tissue samples was preserved in neutral buffered 10% formalin, embedded in paraffin, sectioned at 2-6 µm and stained with haematoxylin and eosin for histological examination. Sections of formalin-fixed lung (n=25) and mesenteric/pulmonary associated lymph node (n=26) were processed by sectioning and staining with osmium-tetroxide post-fixation technique followed by embedding in paraffin using standard methodology (Fernández et al 2005) to demonstrate fat emboli. Immunohistochemical techniques to demonstrate fibrinogen and myoglobin in skeletal and cardiac muscle and kidney were identical to the techniques described in a study of stranding (capture) myopathy (Herráez et al 2007). The ears (tympanoperiotic complexes) were dissected and preserved in 10% formalin for further microscopic examination. Tympanoperiotic complex (ear) analyses Twenty one pairs of tympanic bullae from the common dolphins involved in the MSE were sent to the University of Kiel for detailed histopathological examination. Of these, five of the freshest have been selected for preferential analysis. Decalcification of the ears is now complete and the fixed material will then be embedded, sectioned and examined, with results due to be produced towards the end of August 2009 (for methodology and further information see Jepson et al 2006)

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Morbillivirus detection Total RNA was extracted from sections of frozen (-80°C) lung (n=26) and brain (n=22) samples and the presence of morbilliviral RNA was tested by reverse transcriptase polymerase chain reaction targeting the conserved N terminus of the morbillivirus N gene (Raga et al 2008). All reactions were conducted in duplicate. Analysis of chemical toxins All tissue samples were collected using standard methodology and stored at –20°C prior to preparation and analysis. Frozen liver samples were analysed for a range of trace elements (Cr, Ni, Cu, Zn, As, Se, Mn, Fe, Ag, Cd, Hg and Pb) and butyltins (monobutyltin, dibutyltin and tributyltin) (mg/kg wet weight). The hepatic molar Hg:Se ratio was also calculated (Law 1992; Jepson 2005; Law 2006). Wet weight concentrations (mg/kg) of 25 individual chlorobiphenyl congeners (IUPAC numbers: 18, 28, 31, 44, 47, 49, 52, 66, 101, 105, 110, 118, 128, 138, 141, 149, 151, 153, 156, 158, 170, 180, 183, 187, 194) and a range of organochlorine pesticides and metabolites were determined in blubber samples according to previously established and validated protocols using internationally standardised methodologies (see Law 1994; Jepson 2005; Jepson et al 2005; Law 2006). The sum of the concentrations of the 25 CB congeners (Σ25CBs) and organochlorine pesticides tested were determined were then converted to a lipid basis (mg kg-1 lipid) using the proportion of hexane extractable lipid (%HEL) in individual blubber samples. Analysis of algal toxins Frozen samples (-80°C) of liver were analysed for the presence of harmful marine algal toxins using high performance liquid chromatographic techniques deployed for the purpose of toxin monitoring in commercial shellfish. For amnesic and paralytic shellfish poisoning toxin groups (ASP and PSP), liquid chromatographic (LC) methods were applied with photodiode array detection [for ASP see Quilliam et al (1995)] and fluorescence detection [for PSP see Anon. (2005) and Turner et al (in press)]. LC with tandem mass spectrometric (MS/MS) detection was also used to confirm any analytical observations from these initial analyses (for ASP; Hess et al 2005). For the diarrhetic shellfish poisoning (DSP) toxins as well as other, co-extracted lipophilic toxins, a LC-MS/MS method was also applied following Gerrsen et al (2008). The range of ASP toxins included domoic acid (DA) and its associated isomers – epi-DA, isoDA-A, isoDA-D and isoDA-E. The targeted toxins of the DSP were okadaic acid (OA), the dinophysistoxins (DTX1, DTX2 and acyl esters of OA and DTXs), pectenotoxins 1, 2 and 11, azaspiracids (AZA1, AZA2 and AZA3), yessotoxin (YTX) compounds - YTX, homo YTX, 45 OH YTX and 45 OH homo YTX and representatives of the cyclic imine groups - 13-desmethyl spirolide C (SPX1) and gymnodimine. For the PSP group, the following toxins were included - saxitoxin (STX) and its derivatives neosaxitoxin (NEO), gonyautoxins (GTX) 1 to 5, decarbamoyl (dc)STX, dcGTX2,3 and the N-sulphocarbamoyl gonyautoxins –2 and –3 (C1 and C2) toxins.

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Table 1 Live sightings of common (D. delphis) and bottlenose dolphins (T. truncatus) in or near Falmouth Bay, Cornwall (5-9 June 2008)

1-“

milling” is typical pre-stranding behaviour as described by Geraci and Lounsbury (1993). This includes a single, cohesive pod swimming in tight circles accompanied by frequent behaviours such as spy hopping, fluke slapping, and audible vocalizations.

BDMLR = British Divers Marine Life Rescue CWTMSN = Cornwall Wildlife Trust Marine Strandings Network

DATE SPECIES LOCATION GROUP SIZE

TIME NOTES OBSERVER

5 June D. delphis Porthoustock, Falmouth Bay 50 N/A ½ mile east of Porthoustock. Lots of activity - gannets diving Orca Seasafaris

5 June D. delphis Off Port Mellon, Chapel Point 30 N/A / CWTMSN

5 June D. delphis Mevagissey (E of Falmouth Bay) 40 N/A Pod had been feeding off Polstreath and were heading SE toward Chapel Point

Marie Pearce

5 June D. delphis Off Penzer Point (W of Mousehole), Mount's Bay

5 14.31 Feeding and playing around boat Duncan Jones Marine Discovery

7 June D. delphis Off The Manacles, Falmouth Bay 30-40 14.02 200 metres off coastline Orca Seasafaris

7 June D. delphis Helford River, Falmouth Bay 2 11.30 Free swimming CWTMSN

7 June D. delphis Mouth of Helford River, Falmouth Bay 2 15.10 Free swimming CWTMSN 7 June T. truncatus Hand Deeps Reef, off South coast

Cornwall 4+ N/A Feeding around fishing boat CWTMSN

8 June D. delphis Off Portscatho, Cornwall 50-60 14.30 Free swimming about 0.25 miles or less offshore CWTMSN

8 June T. truncatus Falmouth Bay, Cornwall 2 17.22 / Royal Navy MMO

9 June D. delphis Porth Creek, a tributary of the Percuil River, Cornwall

7 08.20 Rescued and returned to deep water by BDMLR and others. (25 other common dolphins died/euthanized in Porth Creek)

BDMLR/CWTMSN

9 June D. delphis Porth Creek 5-7 08.20 Free swimming, milling behaviour1, later herded out to sea BDMLR/CWTMSN

9 June D. delphis Mouth of Porth Creek 20-30 08.20 Free swimming, milling behaviour1, later herded out to sea BDMLR/CWTMSN

9 June D. delphis Place, at the mouth of the Percuil River, Cornwall

1 35-40

08.15 AM

One dolphin stranded (later refloated). Free swimming, milling behaviour

1, later herded out to sea

BDMLR/CWTMSN

9 June D. delphis Inner part of Falmouth Harbour, Cornwall (approx 5km due west from Porth Creek)

15 09.30 Free swimming, milling behaviour1, two attempted to strand,

ignored boats/humans, resisted attempts to shepherd them out to sea. Dolphins later swum back to sea overnight.

BDMLR/CWTMSN

9 June D. delphis Gillan Creek, Falmouth Bay, Cornwall 12 16.30 Free swimming, milling behaviour1, seven attempted to

strand, herded back to sea BDMLR/CWTMSN

9 June D. delphis Trelissick (approx. 6.5km NNW of Porth Creek) in the River Fal

1 16.30 Live-stranded, euthanized BDMLR/CWTMSN

11 June T. truncatus Mounts Bay, Cornwall 2 12.18 Playing around a wildlife tour boat CWTMSN

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5 Results The locations of the live and dead dolphins reported in this MSE are shown in Figures 1 and 2. The temporal distribution of all common dolphin strandings recorded in Cornwall in 2008 is shown in Figure 3.

Common dolphin strandings in Cornwall by day (2008)

11 11 121 1

4

1 1 1 1 1 1 1 1 1 1 1 11 1 12

26

0

5

10

15

20

25

30

01/01/08 01/02/08 01/03/08 01/04/08 01/05/08 01/06/08 01/07/08 01/08/08 01/09/08 01/10/08 01/11/08

Date

No.

Figure 3 All common dolphin strandings (live and dead) in Cornwall (by day) in Jan-Dec 2008. (Data: CWTMSN).

Gross and histopathological examination of 26 dead common dolphins Twenty-six common dolphin carcasses (12 juvenile males, 7 juvenile females, 6 adult females, 1 adult male) were retrieved from the MSE. Each was subjected to gross necropsy using standardised methodologies (Jepson 2005) (Table 2). The main gross and microscopic findings were similar in all cases. All dolphins appeared to be in good body condition and showed no evidence of acute physical injury or disease that might have precipitated the MSE. No acute traumatic lesions characteristic of by-catch (Kuiken et al 1994), boat impact (Jepson 2005) or bottlenose dolphin attack (Ross and Wilson 1996; Jepson and Baker 1998; Jepson 2005) were seen in any of the dead (or surviving) common dolphins. One dolphin had a chronic injury (associated with granulation tissue and localised fibrosis) on the rostral tip of the maxillae (upper beak) that was considered relatively minor significance to the overall health of the animal. Low intensity parasitic infestations were typical, most frequently in lungs, and these were associated with relatively mild host tissue reactions commonly found in stranded common dolphins in UK waters (Kuiken et al 1994; Jepson 2005; Jepson et al 2005). There was generalised congestion of viscera and the stomachs were free of recently-ingested prey in all cases. Eleven dolphins had moderate to copious quantities of muddy substrate in the trachea and bronchi. Particulate matter (mud) and plant material could be seen microscopically in some bronchial, bronchiolar and alveolar spaces, indicating asphyxiation due to inhalation

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of mud and/or water as the most probable cause of death of these dolphins. In other cases, generalised visceral congestion and degenerative lesions in skeletal and cardiac muscle (acute rhabdomyolysis) and kidney (acute renal cortical tubular necrosis) were consistent with acute cardiovascular failure and stranding (capture) myopathy associated with stress-related events such as capture and beach stranding, as described in the striped dolphin (Stenella coeruleoalba) (Herráez et al 2007). However, immunohistochemical studies using anti-myoglobin antibodies (Herráez et al 2007) demonstrated minimal to absent myoglobinuric nephrosis and myoglobinuria in formalin-fixed kidney samples. These findings indicate that all 26 dead dolphins examined probably stranded alive and died relatively quickly afterwards. Specific gross and microscopic examination of the cerebrum, cerebellum and spinal cord failed to detect inflammatory or infectious processes in any of the animals examined (n=26) (Table 2). A small number of gas bubbles were seen in the mesenteric veins of some fresh carcasses but other tissues were generally free of macroscopic or microscopic bubbles. Intravascular bubbles were seen in some of the more-decomposed carcasses, but these were considered to be consistent with post-mortem change rather than ante-mortem gas embolism. Lung and lymph node samples were negative for the presence of fat emboli in all 26 dolphins examined. The ears (tympanoperiotic complex) were free of parasites and grossly normal in all cases, apart from two dolphins that had silt lining the outside of the tympanic bullae. Bacteriological findings Bacteriological findings were unremarkable and, microscopically, there was no evidence of host reaction to bacterial organisms, indicating only probable post-mortem colonisation of tissues. The bacterium Brucella ceti, which has been associated with lesions in cetaceans (Foster et al 2002), was isolated from a grossly and microscopically normal sample of testis from a single juvenile dolphin, but this bacterium was not isolated from any other tissues from this animal.

Morbillivirus detection There was no evidence of morbillivirus RNA in lung (n=26) or brain (n=22) samples tested by reverse transcriptase polymerase chain reaction (RT-PCR) (Table 2). Chemical and algal toxin detection Analyses of frozen blubber samples from the adult dolphins (six female, one male) determined mean levels 10.7 mg/kg lipid weight (range: 2.80-30.6) for the sum of 25 chlorinated biphenyls (Σ25CBs). Mean concentrations (mg/kg lipid weight) were 0.17 (range: 0.05-0.45) for ppDDT; 0.86 (0.13-2.86) for ppDDE; 0.09 (0.02-0.23) for ppTDE, 0.01 (0.011-0.014) for alpha-hexachlorocyclohexane; <0.01 (all cases were below limit of analytical detection) for gamma-hexachlorocyclohexane; 0.02 (0.01-0.04) for dieldrin and 0.05 (0.01-0.04) for hexachlorobenzene. Analyses of frozen liver tissues from same the adult animals (six female, one male) determined mean concentrations (in mg/kg wet weight) of 31.9 (range: 9.20-53.0) for Hg; 0.29 (0.10-0.50) for Cd; 0.03 (0.02-0.03) for Pb; 0.08 mg/kg (0.07-0.11) for Cr; 3.14 (2.70-3.80) for Mn; 168.1 (109.0-221.0) for Fe; 0.07 (0.05-0.08) for Ni; 6.40 (5.40-7.90) for Cu; 49.6 (40.0-90.0) for Zn; 0.36 (0.28-0.43) for As; 13.8 (5.40-22.0) for Se and 1.41 (0.72-2.60) for Ag. The molar Hg:Se ratio was less than 1.0 in all common dolphin livers examined. The mean concentration of the summed hepatic concentrations of

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monobutyltin, dibutyltin and tributyltin was 0.03 (range: 0.021-0.054) mg/kg wet weight. Using toxicological data from adult female UK-stranded common dolphins in 1990-1992 for comparison (Kuiken et al 1994; Law 1994), mean levels of all organochlorine contaminants examined in both periods (including Σ25CBs; Figure 4) were lower in the adult common dolphins in the Cornwall MSE in 2008 than in dolphins from the 1990-1992 period. Using the same two groups of toxicological data both this time restricted to adults of both sexes, mean hepatic concentrations of all butyltins and Cr, Ni, Cu, Zn, As, Se, Ag, Cd, Hg and Pb were again lower in the dolphins from the MSE in 2008 than in the 1990-1992 group. No toxicological data were available for comparison from the 1990-1992 period for Mn, Fe and Ag. Analyses of frozen liver tissues from the adult animals (six female, one male) were negative for the presence of a suite of algal toxins including neurotoxic compounds e.g., domoic acid and saxitoxin, and also for toxins known to cause gastrointestinal disturbance including okadaic acid and dinophysis toxins (Table 2).

Figure 4 Mean summed 25CBs levels in UK-stranded adult female common dolphins from 1990-1992 (n=8) and from the MSE in 2008 (n=6). Bars=2 S.E.

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Table 2 Pathological data and diagnostic test results on 26 common dolphins examined at necropsy SW reference number

Sex Age class

Nutritional condition

Food in stomach

Significant pre-existing disease

Evidence of trauma (e.g. by-catch)

Gross examination of ears

Brucella sp. infection

Gas embolism

Fat emboli

Morbillivirus infection

Algal toxins (liver)

Chemical toxins

SW2008/94.1 M Juvenile Good negative negative negative normal - no parasites negative negative negative negative not tested not tested

SW2008/94.2 F Juvenile Good negative negative negative normal - no parasites negative negative negative negative not tested not tested



SW2008/94.5 F Adult Good negative negative negative normal - no parasites negative negative negative negative negative tested*

SW2008/94.6 M Adult Good negative negative negative normal - no parasites negative negative negative negative negative tested*




















SW2008/95 M Juvenile Good negative negative negative normal - no parasites Brucella ceti (testis only)

negative negative negative not tested not tested

*- see “Chemical and algal toxin detection” section of results for further information

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Disturbance by marine noise The hypothesis that marine noise coincident with the strandings could have been responsible for the MSE was considered. There were no acoustic recordings at the time of the stranding to assess background sound levels. Information on high-intensity acoustic activities in the general vicinity of the MSE showed that the nearest earthquake to the stranding date and location was recorded off the coast of northern France near Le Havre (approximately 330 km from Cornwall), 2.8 ML magnitude at 10 metres of depth on 30 May 2008 (source: European-Mediterranean Seismological Centre) (Figure 5). The UK Department of Energy and Climate Change (DECC) confirmed that no geophysical surveys, including surveys involving seismic methodologies, were licensed to take place in the English Channel or Southwest Approaches, or in any adjacent sea area, either prior to or during the stranding event. A research vessel (RV Celtic Explorer) was conducting a high-resolution 2-D seismic survey in the Celtic Sea south of Cork, using a relatively small sized array of 150 cubic inches (commonly arrays can exceed 3000 cu inches for 2-D surveys), from 31 May until 14 June at a distance from the MSE of over 200km with intervening land (data: Marine Institute) (Figure 5). Falmouth Harbour Authority records show no unusual commercial shipping movements in or out of the harbour prior to the MSE. No record of movements of small pleasure craft or the use of non-military sonars exists, but no particular large-scale events likely to cause significant noise inputs (e.g. a powerboat race) occurred in the relevant period. A commercial dockyard exists in Falmouth harbour within the estuary. The dockyard is mainly a dry dock and the management reported no unusual activity around this time. A naval exercise involving up to 20 Royal Navy surface and submarine vessels and 11 vessels from seven other countries (Holland, France, Germany, USA, Belgium, Chile and Denmark) was conducted in the South Coast Exercise Area off the southern coastline of Cornwall, Devon and Dorset from 1-9 June, with peak activity on 4-5 June (see Figures 5 and 6) (data: UK Ministry of Defence). Detailed information was supplied by the UK Ministry of Defence on acoustic activities of naval vessels and aircraft of all nationalities that were taking part in the exercise during the period 1-9 June 2008. During the period from 1 June until the afternoon of 9 June, intermittent and occasional acoustic outputs from naval vessels were reported, including the use of standard echosounders (35/50/200kHz), other sonars, acoustic modems, autonomous sonobuoys, and the firing of live, inert and blank ammunition, including a single live Seawolf missile (data: UK Ministry of Defence). Antisubmarine warfare (ASW) activities using mid-frequency sonars (2-4 kHz and 5-8kHz) were conducted in the areas Foxtrot, Golf and Hotel (Admiralty Chart 442) at least 45-50km from the stranding locations in Falmouth Bay (Figure 5) up to 6 June, some 60 hours before the discovery of the stranded dolphins. On 8 June, a high frequency side-scan sonar (100kHz) was towed near the surface in an area between 15 and 50 km approximately from the location of the MSE and conducted between 10:00-14:32hrs (Figure 5). A submarine was operating in the Southern Exercise Area, including Falmouth Bay, on the 8 June and from 0900–1500hrs on 9 June using an echo sounder (at 50 KHz) and passive sonar. A low-power (70 Watts) short range underwater telephone (8kHz) was scheduled to be used on 9 June (Figure 6) but this device was only used in the Plymouth area and was not used until after the dolphins had first started to strand at Porth Creek (data: UK Ministry of Defence). The unspecified echo-sounder deployed on 9 June (Figure 6) was a standard navigational system deployed on a troop carrier (RNLN Amphibious Ship Johan De Witte) in the vicinity of Plymouth.

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A helicopter flying exercise (not anti-submarine warfare) was scheduled to take place between 08:00-13:30hrs on 9 June in the Falmouth Bay (North), Falmouth Bay and Mounts Bay areas. The Falmouth Bay area on 9 June was allocated to RNAS Culdrose Squadrons (Royal Navy helicopter base), but the first flight to leave RNAS Culdrose was at 08:58hrs on 9 June (37 minutes after the MSE was first reported to Falmouth Coastguard). This helicopter returned to RNAS Culdrose at 09:31hrs and the first incoming flight inbound from Netheravon landed at RNAS Culdrose at 09:17hrs (around 1 hour after the discovery of the MSE) and did not use the Falmouth Bay area. There were no helicopter flights from UK or non-UK naval ships in the Falmouth Bay region prior to the onset of the MSE and no sonar of any type was deployed by the helicopters (data: UK Ministry of Defence). Naval activities incorporating anti-submarine mid-frequency dipping sonars and firing of inert rounds resumed on the afternoon of 9 June (data: UK Ministry of Defence). The airspace in the vicinity of St Mawes is uncontrolled and available to all civilian aircraft and such aircraft do not need to file a flight plan or utilise an air traffic service (data: Civil Aviation Authority) and so the possibility that civil aircraft were in the vicinity cannot be discounted.

Figure 5 Distribution of high-intensity acoustic activities nearest to stranding location

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Figure 6 Temporal distribution (5-9 June) of naval acoustic activities and possible bottlenose dolphin (Tursiops truncatus) sighting in western part of South Coast Exercise Area

Disturbance by other cetacean species The nearest reported sightings of killer whales (Orcinus orca) to the MSE were in waters off west Wales on 1 June 2008 and off northern Scotland on 7-8 June 2008 (data: Janet Baxter pers com.; Seawatch Foundation). An unconfirmed report of two bottlenose dolphins (Tursiops truncatus) in Falmouth Bay was made by naval Marine Mammal Observers (MMOs) at 17:22hrs on 8 June. Other confirmed and unconfirmed reports of bottlenose dolphins were made within 25km of Falmouth Bay both before and after the MSE (Table 1). These are consistent with the presence of a small group of inshore bottlenose dolphins that is known to have been continuously resident around the southwest peninsula, including this area, since 1991 (data: Cornwall Wildlife Trust). Geographical and other factors The strandings were in shallow, tree-lined, narrow tidal creeks with muddy substrates where common dolphins are not normally seen. Only two entries among 7,700 cetacean sightings records held by the Cornwall Wildlife Trust were from this area and involved two common dolphins that stranded alive at different times in different tributaries of the Fal. Common dolphins are frequently present in the open bay, although usually two kilometres or more from the shore (data: Ray Dennis pers com./Cornwall Wildlife Trust Marine Sightings Database). There were no reports from local fisheries of unusual fish distribution or fish die-offs in the Falmouth Bay region (data: Cornwall Sea Fisheries Committee).

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6 Discussion Prior to the MSE in Falmouth Bay on 9 June 2008, only three common dolphin MSEs, all of undetermined cause, have been recorded in the UK. One of these MSEs consisted of five dolphins on 3 November 1915 at Tean, Isles of Scilly; another, of five animals near Invergordon, Ross and Cromarty on 8 February 1937, and a third involved 15 dolphins near Pembroke, Wales on 11 August 1938 (listed by Van Heel 1962). Since 1990, over 500 systematic post-mortem examinations have been conducted on single UK-stranded common dolphins (over 275 of them from Cornwall), with the majority determined to have died due to incidental capture in commercial fishing gear (by-catch) (Kuiken et al 1994; Jepson 2005). These by-catch events, in which mainly dead stranded animals are scattered widely, are very different both spatially and temporally, from the MSE reported in the present study. Based on the times of high and low water, it is possible that the common dolphins entered the inner parts of Porth Creek (where they were first discovered) either after 06:30-07:00hrs on 9 June or sometime shortly after 00:00hrs on 9 June. All of the dead dolphins retrieved for necropsy in Porth Creek were found below the extremities of the bank (i.e. below high water level) suggesting that they had not been in the creek at high tide (dead or alive) but may have entered and died on the rising tide after 06:30-07:00hrs on 9 June. The presence of water and mud in their lungs in a number of dead dolphins is also consistent with them stranding alive on a rising tide. Based on 18 years of necropsies of UK-stranded and by-caught cetaceans, seawater is rarely, if ever, found in the lungs of porpoises and dolphins that have died of asphyxiation (by-catch) in fishing nets, demonstrating that water is not aspirated during by-catch and that the blowhole is closed after death so that seawater is usually unable to enter the lungs even when the carcass is underwater (in a net) and at considerable depth (Kuiken et al 1994; Jepson 2005). In contrast, seawater in the lungs is usually only seen on necropsy in some UK-stranded cetaceans that have stranded alive (most probably on a rising tide) where the rising water level eventually submerges the blowhole of the live-stranded animal resulting in drowning by terminal inhalation of seawater (UK CSIP Pathology Database/P.D. Jepson, pers obs). A similar mechanism (stranding alive on a rising tide) is likely to explain the water and mud found in the lungs of 11/26 dead dolphins in this MSE. Evidence of acute cardio-respiratory failure or acute rhabdomyolysis (stranding myopathy) without significant myoglobinuria in the common dolphins found dead on 9 June is consistent with the dolphins entering Porth Creek alive and dying relatively quickly afterwards. Diseases such as stress cardiomyopathy (Cebelin and Hirsch 1980), capture myopathy (Spraker 1993) and contraction band necrosis (Turnbull and Cowan 1998) may cause rapid death in mammals exposed to extremely stressful events (such as capture, violent assault or beach stranding), with cetaceans appearing particularly vulnerable to these conditions (Clark et al 2006). Based on tide times, state of decomposition and pathological findings, the dolphins most probably entered Porth Creek sometime after 06:30-07:00hrs and before 08:21hrs on Monday 9 June, although entry to the creek sometime after midnight on 9 June cannot be excluded. No acute traumatic external or internal lesions consistent with by-catch (Kuiken et al 1994; Jepson 2005) were found in any of the dolphins. By-caught common dolphins usually have food in their stomachs (Kuiken et al 1994; Jepson 2005) and the absence of stomach contents in the examined dolphins in this MSE probably rules out a hazardous pursuit of prey as the cause of this event. Attacks by bottlenose

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dolphins are known to kill porpoises and produce distinctive external and internal injuries but none of these characteristic lesions (Ross and Wilson 1996; Jepson and Baker 1998; Jepson 2005) were seen in any of the dead or surviving common dolphins or in video footage of the live animals. A small group of bottlenose dolphins is known to have been continuously resident around the southwest peninsula, including this area, since 1991 (data: Cornwall Wildlife Trust), so the coincidence of the two species is not unusual. No MSE has ever been causally linked to negative interactions by bottlenose dolphins, however there are seven records of individuals of four species of cetacean (including two common dolphins in 2008) that stranded singly in southwest England since 1992 and exhibited skin rake (teeth) marks and sometimes other injuries consistent with attack from bottlenose dolphins (Barnett et al, in press). A common dolphin mass mortality event in 1994 in the Black Sea (Birkun et al 1999) was linked to distemper caused by cetacean morbillivirus infection and occurred over a much longer period of time than this event. No lesions consistent with distemper were seen in the MSE in Cornwall and all tests for morbillivirus infection were negative. The longstanding theory of a “sick lead animal” that may lead other cetaceans in the social group to strand also appears unlikely here both because no such individual was found among the dead (although one unconfirmed dead dolphin was reported but not retrieved) and because of the fragmented grouping of the live and dead animals. Analytical tests of tissue samples from the seven adults showed that they were free of harmful algal toxins and the levels of organochlorines (polychlorinated biphenyls and pesticides such as DDT), trace metals and butyltins were at relatively low levels and generally lower than levels recorded in stranded common dolphins in south-west England in 1990-92. As the very earliest stages of decomposition were already present in all the dolphins examined subtle inner-ear injuries potentially related to direct high-intensity acoustic exposure (Jepson et al 2006) are likely to be undetectable so, although ongoing, examination of the auditory apparatus would be unlikely to add further information. The rest of the pathological investigation indicates that these animals were healthy until they stranded, but gives no further positive or negative indicators as to the likely cause. For centuries humans have made sounds to induce mass strandings of otherwise healthy small cetaceans in drive fisheries for food (Brownell et al. 2008). High intensity acoustic energy sources were therefore considered as a potential trigger of the MSE. The seismic survey by the RV Celtic Explorer appears to have been too distant, and the earthquake occurred too long before the event to be a likely cause, while nearby dockyard activity was reported to be normal and is therefore unlikely to have attracted animals into its proximity. Military acoustic sources (particularly mid-frequency anti-submarine sonars) have been causally linked with cetacean MSEs predominantly involving beaked whales (Frantzis 1998; Jepson et al 2003; Brownell et al 2004; Fernández et al 2005; Cox et al 2006, Weilgart 2007; Parsons et al 2008, Brownell et al., in press). These events are often described as “atypical” because multiple beaked whales, mainly Cuvier‟s beaked whale (Ziphius cavirostris), strand over a wide geographic area of coastline over a short period of time. It has been proposed that beaked whales (and possibly other cetaceans) may show hazardous behavioural changes in response to some sonar frequencies, potentially leading to nitrogen supersaturation and risk of gas embolism similar to decompression sickness in humans (Jepson et al 2003; Fernández et al 2005; Zimmer and Tyack 2007). The only non-beaked whale MSE causally linked to high-intensity anthropogenic sound

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was a near-MSE of melon-headed whales (Peponocephala electra) in Hawaii in 2004 that most likely resulted from mid-frequency sonar deployed by the U.S. Navy (Southall et al 2006). A behavioural review strengthened the case that mid-frequency sonar played a major role in this near-MSE (Brownell et al., in press) where a group of normally pelagic animals entered a shallow bay very soon after active mid-frequency sonars were deployed nearby. They exhibited “milling” behaviour (Geraci and Lounsbury 2005) and remained (even after the sonar was turned off) until humans finally herded them out of the bay (Southall et al. 2006). Although the naval exercises using active mid-frequency sonars for antisubmarine warfare training (ASW) could have been a factor causing one or more large groups of common dolphins to be closer to shore than normal in the days leading up to the MSE, they were considered highly unlikely to have directly triggered the MSE. Several consecutive days of ASW mid-frequency sonar activity ended on 6 June, some 60 hours before the MSE was first reported. Neither does the pathology in this MSE support a diagnosis of a „decompression sickness‟ type of disease (Jepson et al 2003; Fernandez et al 2005; Jepson et al 2005) or show any gross trauma consistent with intense sound or shock waves (reviewed in Cox et al 2006, Jepson et al 2006; Weilgart 2007; Parsons et al 2008). The towed high-frequency (100kHz) side-scan sonar trial conducted at 10:00-14:32hrs on 8 June was between 15-50km from the location of the MSE and terminated approximately 18 hours before the MSE was discovered. Such high-frequency acoustic devices are commonplace in the marine environment occurring on almost all vessels and, although high-frequency systems are often components of both naval exercises and seismic surveys, they have not been directly implicated (causally) in any cetacean MSEs. One naval activity potentially close enough in time and space to have directly and simultaneously triggered the MSE and caused the agitated behaviours seen in the dolphin groups located very close to shore on the morning of 9 June at Porth Creek, Place and (slightly later) in the inner part of Falmouth Harbour, was the helicopter flying exercise scheduled for Mounts Bay, Falmouth Bay North and Falmouth Bay regions between 08:00 and 13:30 on Monday 9 June. Helicopters generally elicit greater behavioural responses in cetaceans than fixed wing aircraft (reviewed in Richardson et al. 1995; Patenaude et al. 2002) and behavioral responses were generally greater in mothers with calves, in shallow waters, in situations where the initial observed behavior was resting (and travelling in small delphinids) and when the aircraft flew at lower (<500m) altitudes and at smaller lateral distances from aircraft to the animals (reviewed in Richardson et al. 1995, Würsig et al. 1998, Patenaude et al. 2002, Würsig and Richardson 2002). The number of detailed studies on the impacts of aircraft on cetaceans is relatively small and forms part of a wider overall knowledge gap on how cetaceans respond to anthropogenic noise (Nowacek et al. 2007). On 9 June all naval helicopter flights in the Falmouth Bay region were allocated to RNAS Culdrose Squadrons. The first flight recorded to leave RNAS Culdrose (nearest Royal Navy helicopter base) was at 08:58hrs on 9 June (37 minutes after the MSE was reported) and the first incoming flight landed at 09:17hrs (around one hour after the first MSE report) so these flights, or any subsequent ones that day, could not have initially triggered the MSEHowever, naval helicopter activity, or some other unknown factor(s), may have caused the apparently agitated/flight response in the group of dolphins later seen entering the inner part of Falmouth Harbour around

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09:30hrs (approx 80-90mins after the initial discovery of the MSE), although detailed flight records were not available at the time to fully explore this consideration further. Detailed long-term flight records (other than take-off and landing times) are not routinely kept for small civilian aircraft and so it is not possible to identify or exclude any low-flying civilian fixed-wing/rotary flights in the Falmouth Bay region on 8-9 June 2008 (data: Civil Aviation Authority). The low power/short range underwater telephone (8kHz) system scheduled to operate on the morning of 9 June was not used until after the dolphins had started to strand, and was only used in the Plymouth area, so can largely be discounted as a potential cause. The “unspecified” echo sounder deployed on 9 June was a standard navigational echo-sounder also deployed in the vicinity of Plymouth and therefore could not have triggered the MSE. Naval exercises using live munitions, helicopters and fixed-wing aircraft and mid-frequency sonars (deployed from surface ships and helicopters) in the South Coast Exercise Area – which extends from Dorset to Cornwall – occur on about 40 weeks of the year. The Royal Navy uses a range of measures to mitigate potential impacts on cetaceans and other marine mammals including “soft starts” (the gradually progressive ramping up of active sonar source levels to allow cetaceans to move away from the vessel conducting the exercise), use of trained observers (MMOs), and reduction of power when cetaceans are sighted close to a vessel operating sonar transmissions (data: UK Ministry of Defence). The naval mitigation of potential impacts of helicopters and fixed-wing aircraft includes maintaining a 500m minimum flight altitude wherever practicable if any cetaceans are seen on the surface (data: UK Ministry of Defence). The rarity of cetacean MSEs in this area indicates that either normal methods of mitigation of naval impacts on cetaceans in the naval exercise area are generally effective, or the conditions necessary for an acoustically-driven MSE have never previously occur. Finally, the possibility exists that the MSE occurred due to some intrinsic error of “navigation” within a social group of dolphins, rather than as a consequence of a specific trigger inducing an adverse behavioural response. One study has modelled coastlines where low frequency cetacean echolocation signals might be distorted by purely geometric effects (Sundarama et al 2006). Falmouth Bay is not a “hotspot” for cetacean MSEs, however and common dolphin echolocation is at frequencies far higher than those that might fit the model (Sundarama et al 2006). Although sightings of common dolphins are not unusual in coastal waters around Cornwall, it is perhaps unusual to see large groups within 2km of the coastline (data: CWT). Therefore, the sighting of a large group of common dolphins near Portscatho on 8 June, together with other near-shore sightings of a large group of common dolphins on 5 and 7 June (both in the Falmouth Bay area) are consistent with a group of dolphins being in potentially unfamiliar near-shore waters and at increased risk of stranding. The 8-9 June period was also close to the peak of the spring tides and this could have partly influenced the onset of a MSE due to navigational error via the occurrence of rapidly receding tides in the coastal creeks where the MSE occurred.

7 Conclusions In conclusion, a number of potential causes of this MSE can be either excluded or considered highly unlikely. These include distemper (morbillivirus), brucellosis, other

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infectious diseases, gas embolism, fat embolism, boat strike, by-catch, attack from killer whales or bottlenose dolphins, feeding unusually close to shore immediately prior to stranding, ingestion of harmful algal toxins, abnormal weather/climatic conditions and high-intensity acoustic inputs from seismic airgun arrays, recreational craft and natural sources (e.g. earthquakes). A large group of common dolphins was seen unusually close to shore in the days leading up to the MSE and, at least potentially, at increased risk of stranding. This near-shore group of dolphins may have been the group that subsequently mass stranded. The reason that at least one large dolphin group was seen so close to shore shortly prior to the MSE is not known but a range of natural (e.g. foraging closer to shore), anthropogenic (e.g. naval activities leading up to 9 June) or other unknown factor(s) may have played a contributory role. The findings in this MSE were most consistent with an adverse group behavioural response to one or more specific triggers on the morning of 9 June 2008 within an otherwise healthy social group of common dolphins situated unusually close to shore. A period of naval exercises involving a variety of high intensity acoustic sources were conducted around the time of the MSE, but evidence of one of more specific naval activities that tightly coincided in time and space with the likely initial onset of the MSE were absent in all the records of naval activities released under the Freedom of Information Act. An intrinsic “error of navigation” within a social group of common dolphins, or a confluence of additional unknown (natural and/or anthropogenic) factors/sequence of events also cannot be excluded as causal factors in this MSE. Ultimately, a definitive cause for the MSE could not be determined. Greater insight into the causes of any future MSEs may require either a direct observation of the onset, or the emergence of an unusual level of coincidence of MSEs with one or more causal factors. Finally, whilst concerns exist within the scientific community about the veracity of acoustic information provided by some military and industrial sources associated with cetacean strandings (e.g. Frantzis 1998; Parsons et al 2008), the UK Freedom of Information Act (FOI) places a legal obligation on the UK Ministry of Defence and other Government Departments to provide accurate information when requested. Should information be withheld (possibly for reasons of national security) this must be explained and justifications given. In relation to the military activity in the vicinity of the Falmouth MSE, the times and positions of all military sonar transmissions and aircraft flights were provided by the MoD under the FOI Act and no records of sonar transmission or naval flights were withheld. This, together with the cooperation afforded by the MoD, provides a high degree of confidence that all appropriate active sonar and other naval data has been obtained for the Falmouth MSE. A mechanism for the independent verification of industrial/military acoustic data would allay many remaining concerns within the scientific community and enable the investigation of potential environmental impacts of high-intensity man-made acoustic sources in the ocean to progress using empirical, rather than unverified, data. The UK MoD has indicated that it would be willing to explore how such a mechanism could be developed.

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8 Recommendations 1) The UK CSIP should review its protocols and resources to try to improve responses to any future MSEs or unusual mortality events in the UK. 2) There is a need in cetacean science, and when investigating mass strandings events specifically, to address the issue of veracity of acoustic information associated with military and industrial sources. Data provided to this MSE investigation was done under the legally binding Freedom of Information Act (FOI) and all questions were answered without any information/data being redacted. The UK MoD has indicated that it would be willing to explore how a mechanism for the independent verification of military acoustic activity could be developed and this is to be welcomed. 3) Closer links between holders of sightings data (e.g. Cornwall Wildlife Trust, Seawatch Foundation etc), cetacean rescue groups (e.g. BDMLR) and MoD/RN in areas where naval exercises take place would enable naval exercises conducted in UK waters to be aware of any recent changes/trends in cetacean distribution and enable RN to adjust naval exercises/activities if live-stranded cetaceans are being refloated (especially during mass strandings). Such links could be possible in the future through the Joint Cetacean Protocol, a virtual, web-based data portal, which is currently being developed as part of the UK Cetacean Surveillance Strategy.

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9 References Anon. (2005). AOAC Official Method 2005.06. Paralytic shellfish poisoning toxins in shellfish. Pre-chromatographic oxidation and liquid chromatography with fluorescence detection. First Action 2005. Gaithersburg, MD, USA: AOAC International (2005). Barnett, J., Davison, N., Deaville, R, Monies, R., Loveridge, J., Tregenza, N. & Jepson, P.D. Post mortem evidence for bottlenose dolphin (Tursiops truncatus) interactions with other dolphin species in southwest England. Veterinary Record (in press)

Birkun, A. Jr et al. Epizootic of morbilliviral disease in common dolphins (Delphinus delphis ponticus) from the Black Sea. Vet Rec. 144, 85-92 (1999). Brownell, R.L. Jr, Nowacek, D. P. and Ralls, K. Hunting cetaceans with sound: a worldwide review. J. Cet. Res. and Man. 10, 81-88 (2008). Brownell, R.L. Jr, Ralls, K., Baumann-Pickering, S. and Poole, M.M. Behavior of Melon-Headed Whales Near Oceanic Islands Mar. Mam. Sci. (in press) Brownell, R. L., Jr., Yamada, T., Mead, J. G. and van Helden, A. L. Mass Strandings of Cuvier‟s Beaked Whales in Japan: U.S. Naval Acoustic Link? International Whaling Commission SC/56E37. (2004). Cebelin,M. S. and Hirsch, C. S. Human stress cardiomyopathy: myocardial lesions in victims of homicidal assaults without internal injuries. Human Pathology, 11, 123-132 (1980). Clark, L. S., Cowan, D. F. and Pfeiffer, D. C. Morphological changes in the Atlantic bottlenose dolphin adrenal gland associated with chronic stress. J. Comp. Path. 135, 208-216 (2006). Cloeckaert A. et al. An IS711 element downstream of the bp26 gene is a specific marker of Brucella spp. isolated from marine mammals. Clin. and Diag. Lab. Immunol. 7 835-839 (2000) Cloeckaert A. et al. Classification of Brucella spp. isolated from marine mammals by DNA polymorphism at the omp

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Cox, T.M. et al. Understanding the Impacts of Anthropogenic Sound on Beaked Whales. J. Cet. Res. and Man. 7, 177-187 (2006). Department of the Environment and Heritage, 2005. Marion Bay whale stranding. Department of the Environment and Water Resources, Australian Government. http://www.environment.gov.au/coasts/publications/marion-bay-strandings-2005.html Fernández, A. et al. „„Gas and Fat Embolic Syndrome‟‟ Involving a Mass Stranding of Beaked Whales (Family Ziphiidae) Exposed to Anthropogenic Sonar Signals Vet. Path. 42, 446-457 (2005). Foster, G. et al. A review of Brucella sp. infection of sea mammals with particular emphasis on isolates from Scotland Vet. Microbiol. 90 563-580 (2002) Frantzis, A. Does acoustic testing strand whales? Nature 392, 29 (1998). Geraci, J. R. and Lounsbury, V.R. Marine Mammals Ashore: A Field Guide for Strandings, 2

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National Aquarium in Baltimore, Baltimore, MD, 305 pp. (2005) Gerrsen, A., Mulder, P. P. J., McElhinney, M. A. and de Boer, J. Liquid chromatography mass spectrometric method for the detection of marine lipophilic toxins under alkaline conditions. J. Chromatogr. A. doi:10.1016/j.chroma.2008.12.099 (2008). Herráez et al. Rhadomyolysis and Myoglobinuric Nephrosis (Capture Myopathy) in a Striped Dolphin J. Wild. Dis. 43, 770-774 (2007)

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10 Glossary of Terms and Acronyms BDEs Polybrominated diphenyl ethers, a class of compounds used predominantly as flame retardants BDMLR British Divers Marine Life Rescue By-catch Incidental catch of non-target species during fishing activity Cetacean Any of various marine mammals of the order Cetacea- whales, dolphins, and porpoises CEFAS Centre for Environment, Fisheries and Aquaculture Science CSIP UK Cetacean Strandings Investigation Programme CWT Cornwall Wildlife Trust Marine Strandings Network Defra The Department for Environment, Food and Rural Affairs Epizootic A rapidly spreading disease which affects a large number of animals in a particular region at the same time Haemorrhage A large flow of blood from one or more damaged blood vessels Histology The study of tissue sectioned as a thin slice Histopathology The microscopic study of diseased tissue. IoZ Institute of Zoology JNCC Joint Nature Conservation Committee Mass stranding When two or more cetaceans (excluding mother-calf pairs) of the same species strand at the same time and location MEM Marine Environmental Monitoring MoD UK Ministry of Defence MSE Mass stranding event Necropsy An examination and dissection of a dead body to determine the cause of death or the changes produced by disease NHM Natural History Museum OCs Organochlorine pesticides (e.g. DDT‟s, dieldrin etc) Pathology The science or study of the origin, nature and course of disease PCBs Polychlorinated biphenyls (organochlorine pollutants) Ria A drowned river valley SAC Scottish Agricultural College (Inverness) SFSC Southwest Fisheries Science Centre, USA SG Scottish Government Stranding Where a cetacean swims, is left by a receding tide or is deposited onto land (beach, mudflats, sandbank etc) dead or alive. Toxicology The science or study of poisons Tympanoperiotic Middle and inner ear and surrounding bony structures complex ULPGC Universidad de las Gran Palmas Gran Canaria UME Unusual Mortality Event. Defined within the US Marine Mammal Protection Act as “A stranding that is unexpected; involves a significant die-off of any marine mammal population; and demands immediate response”. VLA Veterinary Laboratory Agency, Truro WAG Welsh Assembly Government WVIC Wildlife Veterinary Investigation Centre, Cornwall Zoonosis An infectious disease of animals that can be transmitted to humans

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11 Acknowledgements This investigation was conducted by the UK Cetacean Strandings Investigation Programme (CSIP) and funded by the UK Department of the Environment, Food and Rural Affairs (Defra). We would like to thank the members of the CSIP Steering Group, particularly the contract manager within Defra (Jo Myers), for their comments and advice during the period of this report. The UK Ministry of Defence and Cdr Andy Robinson and Lt Cdr Lez Hardy (Royal Navy) provided detailed information and comments on acoustic inputs into the marine environment from Royal Navy vessels/activities involved in the South Coast Exercise Area during the period 1-9 June 2008 along with comments on the structure and content of the report. Individuals and organisations that contributed information and comments to support this investigation and report include Jeff Loveridge (Cornwall Wildlife Trust Marine Strandings Network) and Dave Jarvis (British Divers Marine Life Rescue), Lesley Jarvis (BDMLR) and Debs Wallis (CWT MSN). Characterisation of the Brucella ceti isolate was conducted by Claire Dawson, Brucella Department, Veterinary Laboratories Agency, Weybridge UK. Data on the event were also provided by British Divers Marine Life Rescue, Cornwall Wildlife Trust Marine Strandings Network, RNLI Falmouth, Marine Coastguard Agency (Falmouth) the residents of Gillan Creek and a range of other agencies and members of the public. Sightings data were provided by Ray Dennis (Cornwall Wildlife Trust Sightings Database Coordinator). Useful scientific information was also provided by Sarah Dolman (Whale and Dolphin Conservation Society). Constructive comments on earlier drafts of this report were kindly provided by Andrew Brownlow (Scottish Agricultural College, Inverness), Peter Tyack (Woods Hole Oceanographic Institute, MA, USA) and several anonymous scientific reviewers. Finally, the events of 9th June 2008 involved and affected a huge number of people. We would like to pay special tribute to those who worked tirelessly during the numerous rescues throughout the day that led to a large number of dolphins being successfully returned to open water, in particular members of British Divers Marine Life Rescue, Cornwall Wildlife Trust Marine Strandings Network and the RNLI. Finally we would like to thank Conrad Birnie, Seth Neil and local members of public in and around Froe for their generous hospitality and unstinting efforts throughout 9th-10th June.

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