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The Stranding Anomaly as Population Indicator: The
Case of Harbour Porpoise Phocoena phocoena in NorthWestern Europe
H elene P eltier1'2*, Hans J. B aagoe3, Kees C.J. C am phuysen4, Richard Czeck5, Willy D abin2, Pierre D aniel6,
Rob D eaville7, Jan H aelters8, Thierry Jauniaux8'9, Lasse F. J en sen 10, Paul D. J ep so n 7, G uido O. Keiji11,
Ursula S ieb ert12, Olivier Van C anneyt2, V incent R idoux1,2
1 Laboratoire Littoral Environnement e t Sociétés, UMR 7266, Université d e La Rochelle, La Rochelle, France, 2 Observatoire PELAGIS, UMS 3462 - Université d e La RochelleCNRS, Université d e La Rochelle, La Rochelle, France, 3 Zoological Museum, The Natural History Museum of Denmark. University of C openhagen, Copenhagen 0 ,
Denmark, 4 Marine Ecology Departm ent, Royal N etherlands Institute for Sea Research (NIOZ), Texel, The Netherlands, 5 The W adden Sea National Park Authority o f Lower
Saxony, Wilhelmshaven, Germany, 6 M étéo France, Dprevi/MAR, Toulouse, France, 7 Cetacean Strandings Investigation Programme, Institute of Zoology, Zoological
Society o f London, London, United Kingdom, 8 M anagem ent Unit of th e North Sea Mathematical Models (MUMM), Royal Belgian Institute of Natural Sciences (RBINS),
O ostende, Belgium, 9 D epartm ent o f Pathology, Veterinary College, University of Liege, Liege, Belgium, 10 Fisheries and Maritime Museum, Esbjerg, Denmark, 11 Naturalis
Biodiversity Center, Leiden, The Netherlands, 12 Institute for Terrestrial and Aquatic Wildlife Research, University of Veterinary Medicine Hannover, Foundation, Büsum,
Germany
Abstract
Ecological indicators for m onitoring strategies are expected to com bine three m ajor characteristics: ecological significance,
statistical credibility, and cost-effectiveness. Strategies based on stranding networks rank highly in cost-effectiveness, but
the ir ecological significance and statistical cred ib ility are disputed. Our present goal is to im prove the value o f stranding
data as po pulation indicator as part o f m on itorin g strategies by constructing the spatial and tem poral null hypothesis for
strandings. The null hypothesis is defined as: small cetacean d istribu tion and m ortality are uniform in space and constant in
time. We used a d rift m odel to map stranding probabilities and predict stranding patterns o f cetacean carcasses under H0
across the North Sea, the Channel and the Bay o f Biscay, fo r the period 1990-2009. As the most com m on cetacean occurring
in this area, we chose the harbour porpoise Phocoena phocoena fo r o u r m odelling. The difference between these strandings
expected under H0 and observed strandings is defined as the stranding anomaly. It constituted the stranding data series
corrected fo r d rift conditions. Seasonal decom position o f stranding anom aly suggested tha t d rift conditions did not explain
observed seasonal variations o f porpoise strandings. Long-term stranding anomalies increased first in the southern North
Sea, the Channel and Bay o f Biscay coasts, and finally the eastern North Sea. The hypothesis o f changes in porpoise
d istribu tion was consistent w ith local visual surveys, m ostly SCANS surveys (1994 and 2005). This new indicator could be
applied to cetacean populations across the w orld and more w idely to marine megafauna.
C itation : Peltier H, Baagoe HJ, Camphuysen KCJ, Czeck R, Dabin W, e t al. (2013) The Stranding Anomaly as Population Indicator: The Case of Harbour Porpoise
Phocoena phocoena in North-Western Europe. PLoS ONE 8(4): e62180. doi:10.1371/journal.pone.0062180
Editor: Athanassios C. Tsikliras, Aristotle University o f Thessaloniki, Greece
Received January 9, 2013; A ccepted March 18, 2013; Published April 22, 2013
C opyrigh t: © 2013 Peltier e t al. This is an open-access article distributed under the term s of th e Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided th e original author and source are credited.
Funding: This work was funded by a PhD grant (CNRS/Region Poitou Charentes), and hosted by th e University of La Rochelle. The funders had no role in study
design, data collection and analysis, decision to publish, or preparation of the manuscript.
C om peting Interests: The authors have declared th a t no com peting interests exist.
* E-mail: hpeltier@univ-lr.fr
can benefit from the p ro tectio n afforded to the habitats shared
w ith top p re d a to r ‘flagship’ species [2,3,5-8], T h e n e ed a n d
efficacy o f conservation plans m ust be assessed by im plem enting
m on ito rin g program m es.
M o n ito rin g is defined as “ the long term collection a n d analysis
o f re p ea te d observations o r m easurem ents to evaluate changes in
condition a n d progress to w ard m eeting a m an ag em en t objective”
[9]. T h e efficiency o f a m on ito rin g plan is based o n th ree expected
perform ances: ecological relevance, statistical credibility a n d costeffectiveness [10,11], N evertheless, collecting d a ta often rem ains
very expensive, p u ttin g m an a g em e n t objectives at risk [11].
Indicators are therefore bein g used as a sim plification o f recorded
param eters. Indicators are defined as m easures established from
verifiable d a ta th a t include m ore inform ation th a n d a ta them selves
do. As a low cost sim plification o f the m o n ito re d param eters,
Introduction
T o p pred ato rs have long b e en considered as conservation
priorities [1 M ]. T h e generally low resilience o f these species results
from their low fecundity a n d their position a t the top o f food webs
a n d m akes th em m ore susceptible to m an y h u m an -in d u ce d
pressures (direct takes, com petition w ith fisheries, by-catch, bioaccum ulation o f persistent contam inants). B ecause top p red ato rs
rely o n low er trophic levels for their food, their conservation
implies a sustainable m an ag em en t o f th eir prey a n d the
preservation o f ecosystem processes th a t determ in e the develop­
m en t o f forage organism s. Finally, because m ost top p red ato rs
have extensive h om e ranges, their conservation should envisage
large subareas. D u e to their often iconic n a tu re , the presence o f
top p red ato rs can be a lever b y w hich m an y less p o p u lar organism s
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Stranding Anomaly as Population Indicator
indicators allow com m u n icatio n betw een scientists a n d policy­
m akers [4,12-14],
C etaceans in E u ro p e are p ro tec te d b y m an y intern atio n al a n d
n ational regulations (e.g. E u ro p ea n U n io n H ab itats D irective,
M a rin e Strategy F ram ew ork D irective a n d C o m m o n Fisheries
Policy; U S E n d an g e red Species A ct a n d M a rin e M am m al
P rotection Act; the O S P A R C onvention; A SC O B A N S). Several
p a ram ete rs can b e m easu red to provide relevant in form ation on
cetacean p o p u latio n status: absolute ab u n d an c e, relative a b u n ­
dance, distribution, dem o g rap h ic p a ram ete rs a n d health status.
M ost o f these p a ram ete rs (absolute a n d relative a b u n d an c e a n d
distribution) req u ire extensive d a ta to be collected a t sea, generally
a t high costs. H ow ever, the efficiency o f m on ito rin g plans is also
based o n cost-effectiveness, a n d the developm ent o f low-cost
indicators for assessing cetacean po p u latio n status is o f g reat
interest. H ence, the p re sen t study was aim ed to exam ine the
potential o f stranding d a ta to provide indicators for cetacean
populations. F or scientific purposes, the w o rd “ stranding” is
com m only used for either live o r d e ad specim en [15]; in the
p re sen t w ork, w e will only be considering d e ad specim ens w ashed
ashore.
It is com m only acknow ledged th a t stranding d a ta are relatively
inexpensive to collect, because they do n o t rely on the
im plem entation o f expensive field w ork c o n d u cted a t sea (even if
necropsies a n d o th er investigations a n d analyses on carcasses
re m a in expensive). T herefore, m an y attem pts for testing the value
o f strandings as a source o f indicators o f m ortality at-sea have been
m ade, m ostíy for seabirds [16,17], sea otters [18,19], sea turtles
[20-22] a n d cetaceans [23-26]. In several E u ro p ea n countries,
m arin e m am m al strandings have b e en recorded for decades.
S tran d in g d a ta held in n ational data-bases jo in d y constitute one o f
the largest datasets a b o u t cetaceans in E u ro p ea n w aters. T h an k s to
th eir fairly low ru n n in g costs, natio n al stranding schem es have
developed in m ost E u ro p ea n countries a n d cover extensive spatial
(1000 s km coasdine) a n d tem poral (several decades) ranges th a t
are consistent w ith the characteristics o f cetacean populations
(extensive p o p u latio n ho m e ranges, low recovery rates). D u rin g the
last 20 years cetacean stranding netw orks have b e en aim ed at
con trib u tin g m on ito rin g strategies b y collecting d a ta o n inter-alia
spatio-tem poral p a tte rn s o f occurrence, cause o f death, health
status, ecological traits a n d po p u latio n structure [27-32]. N ever­
theless, the use o f stranding d a ta is often lim ited by the
opportunistic n a tu re o f sam pling a n d the difficulty to relate
p attern s a n d figures observed in strandings w ith processes affecting
populations [33]. N onetheless, the scientific use o f strandings as a
source o f p o p u latio n indicators is enco u rag ed b y a variety o f
in tergovernm ental dispositions o r recom m endations (International
W halin g C om m ission; various agreem ents u n d e r the C onvention
for M ig rato ry Species; In tern a tio n a l C ouncil for the E xploration
o f the Sea; O S P A R C onvention; M a rin e M a m m a l P rotection
A c t...). T h erefo re, it becom es p articularly im p o rta n t to delineate
th eir ecological significance a n d statistical credibility.
T h e h a rb o u r porpoise (Phocoena phocoena) is listed in m any
intern atio n al conventions, directives a n d agreem ents (e.g. C onser­
vation o f M ig rato ry Species o f W ild A nim als, E U H ab itats a n d
Species D irective, P rotocol for Special P ro tected A reas a n d
Biological D iversity, C o nvention o n In tern a tio n a l T ra d e in
E n d an g e red Species o f W ild F a u n a a n d Flora, A greem ent on
the C onservation o f Sm all C etaceans o f the Baltic, N o rth E ast
A dantic a n d N o rth Seas (ASCOBANS)) [34], M o n ito rin g h a rb o u r
porpoise populations is requested by a n increasing n u m b e r o f
dispositions, including the A S C O B A N S conservation p lan in the
N o rth Sea a n d recovery p lan in the Baltic Sea. Indeed, the
h a rb o u r porpoise is im pacted by a n th ro p o g en ic disturbances,
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m ostly fishery activities (com petition a n d bycatch) [27,35-40],
organic pollutants a n d heavy m etals c o n tam in atio n [28,41-45]
a n d recently the exponential grow th o f industrial activity a t sea
th ro u g h the construction o f offshore w ind farm s [46,47]. T h e
existence o f pressing c onservation issues a n d the b ro a d distribution
o f the h a rb o u r porpoise in E u ro p e a n w aters p ro m p te d us to
concentrate the p re sen t study o n this species. T h e study a rea
covered the n o rth -eastern A tlantic w aters o f the Bay o f Biscay a n d
the N o rth Sea, hence encom passing a n extensive p a rt o f the
species distribution in E u ro p ea n w aters.
C e ta ce a n strandings follow a com plex function o f a biological
co m p o n e n t th a t is a b u n d an c e a n d m ortality rate, a n d a physical
one th a t is drift processes, including carcass b uoyancy a n d
re p o rtin g conditions.
N stranding ~ Nindividuai.mortality.buoyancy.drift.reporting.
D rift conditions b ein g m ostíy driven by w ind a n d tide are likely
to introduce m u ch noise in stranding d a ta series. H e re we explore
how drift varies spatially a n d tem porally a n d assess its c o ntribution
to v a riation in cetacean stranding num bers. By using the drift
m odel M O T H Y developed by M étéoF rance, the F ren ch m eteo ­
rological agency, w e propose to exam ine how h a rb o u r porpoise
(and b y extension any small cetacean) stranding should be
d istributed if variations w ere only due to drift conditions
(abundance, m ortality ra te a n d re p o rtin g ra te bein g set uniform
a n d constant). As such, we built the null hypothesis (H 0) o f
stranding records a n d m ade predictions o f inter-alia long term
stranding series a n d seasonal variations a t various spatial scales
across study area, against w hich observed stranding d ata, provided
by six contiguous n ational stranding schem es (from n o rth to south:
U K , D en m ark , G erm any, T h e N etherlands, B elgium a n d France)
can be statistically c o m p a red in a rigorous hypothesis testing
pro ced u re. T h e m ain goal o f the c u rre n t study is to im prove the
statistical credibility o f stranding records as indicators for m arin e
m egafauna in a m on ito rin g perspective a t intern atio n al scale. F or
the first tim e in E urope, adm inistrative b oundaries w ere pulled
dow n to w ork a t cetacean pop u latio n scale.
M aterials and M ethods
1-G e n e ra l E x p e r im e n t D esig n
T h e study a re a covered the Bay o f Biscay, the C h a n n el a n d the
N o rth Sea (8 °5 0 'W -1 0 °0 0 'E ; 4 3 ° 0 0 'N -5 9 °0 0 'N ).a n d ran g ed
from 1990 to 2009. Sm all cetacean stranding tim e series a n d
seasonal p a tte rn s calculated u n d e r the null hypothesis reflect
stranding variations expected u n d e r the effect o f tides a n d w ind
only, w ith the assum ption th a t d e ad cetacean occur uniform ly in
tim e a n d space. T h e y w ere co nstructed follow ing four steps
(figure 1).
Firstly, the hypothesis o f spatial a n d tem poral uniform ity o f
de ad h a rb o u r porpoises was rep resen ted by theoretical cetaceans
uniform ly distributed in a g ridded m ap o f the study area. T h e ir
drift was c o m p u ted for 30 day every 10 days from 1990 to 2009,
by using the drift pred ictio n m odel M O T H Y , a n d the value o f 1
was a ttrib u te d to its cell o f origin if it was p red icted to stra n d a n d 0
if n ot. G rid d e d m aps o f 0 a n d 1 w ere built a n d yearly, seasonally
o r m onthly averaged to represent the p robability th a t a cetacean
dying in each cell reaches the coast a n d get stranded, u n d e r the
influence o f tides a n d w ind only (Pstmni,ng)- Finally, these
sim ulations allow ed 20-year-long strandings tim e series to be
p red icted u n d e r the null hypothesis. T hese predictions w ere
c o m p a red to observed strandings along E u ro p ea n coasts in ord er
to highlight differences w ith the hypothesis o f uniform ity in
ab u n d an c e a n d distribution o f d e ad cetaceans, a n d thus underline
the biological co m p o n e n t o f h a rb o u r porpoise stranding records.
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Stranding Anomaly as Population Indicator
CONCEPTS
Sm all cetacean distribution
a nd m ortality are uniform in
„
.
,
, . „
Prediction o f sm all cetacean strandings u n d e r th e in flu en ce o f
space and constant in tim e.
tid es and w ind only.
Probability th at a cetacean
dying in each cell reach es th e
coast.
, ,.
Seasonal clim atology o f
strandings.
METHODS
238 theoretical dolphins
uniform ly distributed.
30 day drift p red icted using
the drift M étéo-France
M O T H Y m odel, ev ery 10
d ays fro m 1990 to 2009.
F o r each theoretical d o lp h in every
10 d ays from 1990 to 2009:
B stranding predicted
no stranding predicted
P robability o f getting
stran d ed g iv en by av erag in g
seasonnal data o v er th e study
period.
C o n stru ctio n o f long term
expected stranding data.
Figure 1. Theoretical scheme o f the experim ent.
d o i:1 0 .1 3 7 1 /jo u rn a l.p o n e .0 0 6 2 1 8 0 .g 0 0 1
O b ject characteristics (thickness a n d buoyancy), date, starting
location a n d d u ra tio n o f the drift are needed. T hese p aram eters
w ere a d a p te d to small cetaceans (size: 2 m; total thickness: 0.32 m;
first (or last in the case o f back-calculation) date a n d location
d o c u m e n ted on a case by case basis), a n d im m ersion ra te was
experim entally estim ated at 90% [26],
Drift calculations. T h e hypothesis o f spatial a n d tem poral
uniform ity o f d e ad porpoises a t sea was rep resen ted by a grid o f
238 theoretical small cetaceans uniform ly distributed cells o f 0.75"
longitude a n d latitude a n d corrected by the pro jectio n distortion
according a n o rth -so u th g radient (figure 1).
Drifts w ere calculated for 30 days every 10 days, from 1990 to
2009. T h e 30 day th reshold was chosen acco rd in g to the
decom position status o f carcasses a n d the change o f im m ersion
ra te at this stage [26],
Stranding climatology. G rid d e d m aps w ere constructed
every 10 days from 1990 to 2009. F or each cell, 1 was a ttrib u te d
if the theoretical cetacean dying in this cell was p red icted to strand
a n d 0 if not. A total o f 720 m aps w ere o btained. T h ey w ere
averaged over 20 years to construct clim atology m aps o f stranding
probability for small cetacean a t various tim e fram es, including
m o n th , season a n d year.
Finally, tim e series o f expected strandings w ere co nstructed w ith
a 10 day resolution, along the E u ro p e a n coast divided in eight subareas (Bay o f Biscay, w estern C hannel, eastern C hannel, south­
w estern N o rth Sea, north-w estern N o rth Sea, south-eastern N o rth
Sea, m id-eastern N o rth Sea a n d n o rth -eastern N o rth Sea). T h e
n u m b e r o f stran d ed cetaceans expected p e r coastal kilom etre per
y ear was a n indicator o f the exposure o f each stretch o f coasts to
small cetacean strandings u n d e r the null hypothesis; in this
exercise coastline was m easu red in straight line along the m ain
o rien tatio n o f each sub-area.
2 -D e fin ition s
W e defined the p robability o f strandings (Pstmndmg) as die
probability th a t a cetacean dying at sea reaches the coast a n d
gets stranded.
E xpected strandings are strandings p red icted u n d e r the
hypothesis o f spatial a n d tem p o ral uniform ity o f d e a d cetaceans.
T h ey vary in tim e a n d space w ith drift conditions only.
O bserved strandings are strandings collected by all E u ro p ea n
stranding netw orks o p eratin g across study area.
T h e difference betw een observed a n d expected strandings was
n a m e d the ano m aly o f strandings. Positive (vs negative) anom alies
suggest th a t m ore (vs less) strandings w ere observed th a n expected
u n d e r the null hypothesis.
W e concluded th a t there was a seasonal p a tte rn (or seasonality),
w hen m onthly num bers o f stranding events averaged over 20 years
show ed m ax im u m (vs. m inim um ) figures d u rin g th ree o r m ore
consecutive m onths.
L ong term d a ta w ere used to describe the 20 y ear tim e series at
eith er an n u al o r m onthly resolutions.
3 -C o n s t r u c ti o n o f t h e Null H y p o th e s i s
Drift prediction model MOTHY. T h e drift o f cetacean
carcasses was m odelled w ith the drift pred ictio n m odel M O T H Y
(Modèle Océanique de Transport d'HYdrocarbures), initially developed by
Météo-France [48] to pred ict the drift o f oil slicks a n d a d a p te d later
o n to solid objects. M O T H Y predicts trajectories o f floating
objects b y calculating the vertical profile o f currents a n d the w ind
effect o n the em erged p a rt o f the object. M O T H Y c an b e used
forw ard (from drift start to lan d in g point) o r back w ard (from
lan d in g location to drift origin) [48].
T h e b a th y m e try used b y M O T H Y was com piled from d a ta
p rovided by S H O M (Service Hydrographique et Océanographique ele la
Marine) at a resolution o f 0.08".
A tm ospheric d ata, p rovided by the E u ro p ea n C e n tre for
M ed iu m -R an g e W e a th e r Forecasts (ECM W F), com bines forecast
outputs a n d d a ta assim ilation processes. T ides are m odelled using
a purely h ydrodynam ic tidal m odel. W ater velocity is gen erated by
a coupling b etw een a 2D hydrodynam ic lim ited a rea ocean m odel
a n d a ID eddy viscosity m odel [48],
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4 - H a r b o u r P o r p o i s e S tr a n d in g D ata
H a rb o u r porpoise stranding tim e series w ere com piled from six
E u ro p ea n countries: D en m ark , G erm any, the N etherlands,
Belgium , E hiited K in g d o m a n d F rance. D ate a n d location o f
strandings, as well as cause o f d e ath w ere collected. Live stranding
events w ere n o t considered as the stranding location is n o t entirely
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Stranding Anomaly as Population Indicator
d e term in ed by drift conditions b u t even by active sw im m ing o f
anim als.
United Kingdom stranding network. T h e stranding n e t­
w ork in the U n ite d K in g d o m is one o f the oldest organisations in
E u ro p e th a t collects d a ta o n stran d ed cetaceans. T h e collaborative
U K C e tacean Strandings Investigation P ro g ra m (CSIP, www.
ukstrandings.org) as it is now know n is a consortium o f p a rtn e r
organizations funded b y D e p a rtm e n t o f E n vironm ent, F ood a n d
R u ra l Affairs a n d the U K D evolved A dm inistrations. P a rtn er
organizations are the Zoological Society o f L ondon, Scottish
A gricultural College (Inverness), the N a tu ral H istory M useum a n d
M a rin e E n vironm ental M onitoring. In C ornw all, strandings d a ta
is collected by the C ornw all W ildlife T ru st M a rin e S trandings
N etw ork a n d necropsies are carried o u t b y the A nim al H e a lth a n d
V e terin ary L aboratories A gency (Truro). T h e C S IP is collectively
tasked w ith recording in form ation o n all cetaceans, m arin e turtles
a n d basking sharks th a t strand a ro u n d U K shores each y ear a n d
w ith the ro u tin e investigation o f causes o f m ortality th ro u g h
necropsy o f suitable strandings. E xperienced pathologists a n d
biologists carry o u t system atic necropsies o f selected stranded
cetaceans follow ing a standardized protocol.
Danish stranding network. T h e D anish stranding netw ork
is ru n b y the D anish N a tu re A gency in collaboration w ith the
Fisheries a n d M aritim e M useum a n d the Zoological M useum ,
N a tu ral H istory M useum o f D en m ark . Post m ortem s on stranded
m arin e m am m als are cond u cted by the N atio n al V eterin ary
Institute. T h e stranding netw ork was founded in 1991 a n d relies
o n official personnel as well as re p o rtin g from the public.
German stranding network. T h e G e rm an stranding n e t­
w ork a t the N o rth Sea coast w as established in 1 9 8 8 /8 9 du rin g the
first P hocine D istem per V irus-Seal-die-off. N atio n al P ark R angers
a n d “ Seal h u n ters” (seals still belong the h u n tin g law even as
h u n tin g was stopped in 1976) control the coastline regularity
th ro u g h o u t the y ear so th a t a regular effort is secured. In
Schlesw ig-H olstein m arin e m am m al carcasses a re collected a n d
subm itted for investigations.
Dutch stranding network. T h e D u tc h strandings netw ork
consists o f a consortium o f a large n u m b e r o f organizations a n d
volunteers. C overage o f the coast is very good along the south­
w estern a n d w estern coasts o f the c o u n try (approaching 100%)
a n d o n the w esternm ost Frisian island o f T exel (coverage
estim ated 80%), b u t ra th e r p o o r in the W ad d e n Sea a n d the
re m a in d e r o f the Frisian Islands, o f w hich som e are u ninhabited.
T h e central digital datab ase is kept by N aturalis Biodiversity
C e n te r (form erly called the N atio n al M useum o f N atu ral H istory
Naturalis) in L eiden. D a ta a n d ph o to g rap h s are m ad e visible o n the
in te rn et (w w w .w alvisstrandingen.nl).
Belgian stranding network. Strandings w ere collected in
Belgium since 1970’s, b u t the dedicated a n d governm ent
supported netw ork was established in 1990. It is organised a n d
centralised by the M a n a g em en t U n it o f the N o rth Sea M a th e ­
m atical M odels (M U M M ), d e p a rtm e n t o f the R oyal Belgian
Institute o f N atu ral Sciences (RBINS). M U M M m aintains, in
coop eratio n w ith the U niversity o f Liège, a single datab ase w hich
can p a rd y be consulted online.
French stranding network. T h e F ren ch stranding netw ork
is co -o rd in ated by the J o in t Service U n it PELAGIS, U M S 3462,
U niversity o f L a R ochelle-C N R S , ded icated to m on ito rin g m arine
m am m al a n d seabird populations, as a c o n tin u atio n o f the
m on ito rin g pro g ram m es form erly know n as the Centre de Recherche
sur les Mammiflres Marins (C R M M ). T h e netw ork is constituted o f
a ro u n d 260 train ed volunteers distributed along the w hole F rench
coast w ho collect d a ta according to a standardized observation
a n d dissection protocol. T h e netw ork was established in the early
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1970 ’s a n d its organisation a n d procedures are considered
u n c h an g e d since the m id 1980’s. D a ta are centralized into a
single database held in L a Rochelle.
5-T im e S eries Analysis
T h e anom aly o f stranding tim e series was built as th e difference
betw een observed a n d expected h a rb o u r porpoise strandings tim e
series. T o do this the expected stranding tim e series was first
calibrated w ith observed stranding tim e series in each large a rea in
o rd e r to o b tain equal cu m u lated n u m b ers in b o th series.
Firsdy, the difference betw een observed a n d expected strandings
was tested by W ilcoxon test for n o n -p a ra m etric p a ire d sam ples, for
each large a re a b o th spatially a n d tem porally. Secondly, the
seasonality o f the stranding anom aly was described over 20 years,
w ith a correlogram p ro d u c ed b y a n a u tocorrelation function
(ACF), using the software R [49,50]. T h is analysis disentangles
seasonal signal a n d trends a n d detects autocorrelations in tim e
series a t different lags. A lag corresponds to the tem poral
resolution o f the tim e series, here one m o n th . In this case, a year
w ould b e rep resen ted by 12 lags. T h e A C F analysis show ed the
degree o f auto co rrelatio n in tim e series a t each lag (from 0 to 24
th a t is two years), a n d revealed the existence o f seasonal signal in
long term series.
C hanges in stranding ano m aly w ere d etected using a n algorithm
for detecting breaks in tim e series, based o n the F-statistics [51].
T his algorithm detects structural changes in a lin ear regression by
testing the regression coefficients a n d can b e applied to tim e series.
6- Ethics S t a t e m e n t
T his w ork reports on new results th a t have never b e en a n d are
n o t being subm itted elsew here. T his w ork was c arried o u t in the
respect o f E u ro p ea n regulation re g ard in g the use o f stran d ed dead
cetacean for scientific a n d conservation purposes. T h e authors
have therefore a d h ere d to general guidelines for the ethical use o f
anim als in research, the legal requirem ents in E urope. N o living
anim als w ere used for this study, only d e ad cetaceans found
stran d ed along E u ro p ea n coasts b y several organisations w ere
considered. N o sam ples w ere used for this study. T h e collect o f
d e ad stran d ed anim als is delegated to regional o r national
organism s u n d e r the perm ission different institutions. In the
U n ited K ingdom , the D e p a rtm e n t o f the E n vironm ent, F ood a n d
R u ra l Affairs is the au th o rity to rem ove anim als for post-m ortem
exam ination. T h e R oyal Belgian Institute is a p p o in ted b y law in
Belgium ; the sam e goes for the N etherlands w here the D u tc h law
is the au th o rity w ho has issued N aturalis the perm ission to collect
stran d ed m arin e m am m als. In L ow er Saxony (G erm any), the
a u th o rity is eith er the N atio n al P ark A uthority W a d d e n Sea o f
L ow er Saxony o r the n a tu re conservation au th o rity o f the county
w ho grants a p e rm it to collect d e ad cetaceans. In Schleswig
H olstein (G erm any), this is the State office for agriculture,
en v iro n m en t a n d ru ral areas. In D enm ark, the relevant a uthority
is the D anish N a tu re Agency, w hich is u n d e r the D anish M inistry
o f the E nvironm ent. Finally in F rance, the M inistry for
environm ent, sustainable d evelopm ent a n d ecology issues the
perm ission to collect strandings to the Pelagis O bservatory
(University o f L a Rochelle).
Results
1-C lim a to lo g y o f Small C e t a c e a n S tr a n d in g E v e n ts in
N o r t h w e s t E u r o p e a n W a te rs
Stranding probability (P stranding). M aps o f stranding
probability w ere constructed, for each season averaged over 20
years (figure 2). Seasons w ere defined on the basis o f the
4
April 2013 I Volume 8 | Issue 4 | e62180
Stranding Anomaly as Population Indicator
strandings p e r coastal kilom etre p e r y ear was calculated. T o
facilitate com parison b etw een large subareas, a n a rb itra ry value o f
1 expected stranding.km 1.year 1 was given to the stretch o f coast
th a t show ed the lowest n u m b e r o f expected strandings, in this case
the south-w estern N o rth Sea coast, a n d figures for the o th er subareas w ere o b tain ed proportionally. H ighest values w ere found in
n o rth -eastern N o rth Sea a n d w estern C h a n n el (7.3 a n d 6.6
stranding.km ’.year 1 respectively; figure 3). Lowest values w ere
found in the n o rth-w estern a n d south-w estern N o rth Sea (1.2 a n d
1.0 stranding.km .year
respectively; figure 3).
Seasonal patterns o f exposure to strandings. M onthly
n um bers in expected stranding in n u m b ers.k m -1 w ere averaged
over 20 years to detect seasonal p attern s in expected tim e series
(figure 4). Seasonality was d etected in the Bay o f Biscay a n d
w estern C h a n n el sub-areas. M ax im a w ere observed betw een
O c to b er a n d F eb ru ary a n d n u m b ers decreased b etw een M ay a n d
A ugust dow n to 34—50% o f the highest num bers. In these three
regions, coefficients o f variations w ere very low (0.27 in the Bay o f
Biscay, 0.25 in eastern C h a n n el a n d 0.13 in w estern C hannel).
Seasonal p attern s along w estern a n d eastern N o rth Sea coasts
w ere opposite, regardless o f n o rth -so u th divisions. In south­
w estern a n d north-w estern N o rth Sea, expected strandings
increased in w inter to reach a m axim um in M a y being m ore
irregular du rin g the rest o f the year. In south-eastern, m id-eastern
a n d n o rth -ea stern N o rth Sea, m on th ly expected strandings w ere
irregular b u t m inim a w ere observed in A pril a n d M ay.
p ro p o rtio n o f cells w ith Pstmndmg = 0 (figure 2). D e cem b er to M a rch
w ere g a th e red together into a w inter season, because all cells w ere
non-null. T h e spring season constituted o f A pril to J u n e , because
cells w ith P strandmg = 0 rep resen ted < 1 0 % o f the study area. Ju ly
a n d A ugust presen ted a p ro p o rtio n o f null cells > 1 0 % a n d
constituted the sum m er season. Finally, m o n th s from S eptem ber
to N ovem ber w ere pooled into an a u tu m n season, because
Pstmndmg = 0 in less < 5 % o f all cells.
T h e probability th a t cetaceans get stran d ed is always h igher in
coastal area.
T h e areas w ith high probabilities o f stranding e x p an d in w inter
a n d shrink in the sum m er as a result o f seasonal variations in
prevailing w ind force. D u rin g w inter m onths only 12.5% o f the
w hole study a rea presen ted Pstm„dmg < 0 .1 . H ighest probabilities o f
strandings (> 0.3) covered 63% o f the study area, over the
continental shelf o f the Bay o f Biscay, the E nglish C h a n n el a n d the
eastern h a lf o f the N o rth Sea. T hese areas re tra cte d d u rin g spring
m onths to 52% a n d a b ro a d a rea o f low stranding probability
a p p ea red in the central N o rth Sea. In the sum m er m onths, a ro u n d
10% o f the study a rea show ed Pstmndmg = 0, suggesting th a t a
cetacean dying in these areas w ould never get stran d ed a n d cells
w ith Pstmndmg > 0 .3 covered no m ore th a n 49% o f the study area.
T hese cells w ere observed over the continental shelf in the Bay o f
Biscay a n d in the w estern h a lf o f central N o rth Sea. A u tu m n drift
conditions show ed Pstmndmg > 0 .3 covering 57% o f the study area.
Exposure of European coasts to small cetacean
strandings. For each large sub-area, the n u m b e r o f expected
L eg e n d
P ro b a b ility of s tra n d in g
I
10 0 1 - 0 10
□
0 .1 1 - 0 .2 0
□
0.21-0.30
H
0.31-0.40
■ ■ 0.41-0.50
H
0.51-0.60
■ ■ 0.61-0.70
■ ■ 0.72-0.80
M
0.81-0.90
M
0 .9 1 -1 .00
B a th y m e try (m)
W inter
-1500
-1000
46°N
-500
-100
I
I Study area
56°N
Sum m er
A utum n
Figure 2. Seasonal maps o f stranding p ro b a b ility in th e study area from 1 990 to 20 0 9. T he d a rk e r th e c o lo u r th e h ig h e r th e p ro b a b ility
th a t a n im a ls d y in g in th e c o rre s p o n d in g cell w o u ld re a c h th e c o a s t.
d o i:1 0 .1 3 7 1 /jo u rn a l.p o n e .0 0 6 2 1 8 0 .g 0 0 2
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Stranding Anomaly as Population Indicator
NWNS= 1.2
MENS= 2.2
SWNS= 1
6°W
4° E
Figure 3. Relative num bers o f expected strandings along th e coasts o f seven large subareas fro m 1990 to 2 0 0 9 (stranding.km
y e a r- 1 ). BB: Bay o f Biscay, WC: w e s te rn C h an n e l, EC: e a s te rn C h an n e l, SWNS: s o u th -w e s te rn N orth Sea, NWNS: n o rth - w e s te rn N orth S ea, SENS: s o u th ­
e a s te rn N o rth S ea, MENS: m id -e a s te rn N o rth Sea, NENS: n o rth - e a s te rn N orth Sea.
d o i:1 0 .1 3 7 1 /jo u rn a l.p o n e .0 0 6 2 1 8 0 .g 0 0 3
stranding.km '.y e a r ') a n d along the eastern C h a n n el coast
(0.03 stranding.km '.y e a r '). T h ere appears to b e good consis­
tency in strandings frequencies across n ational boundaries,
suggesting th a t possible differences in re p o rtin g effort betw een
countries w ould n o t be a m ajo r source o f heterogeneity.
Long term trends in observed harbour porpoise
stranding data. O v e r the w hole study area, porpoise strandings
show ed a strong increase over the study period, m ostly since 2000
(figure 6). T h e m axim um o f 1 240 porpoises was reach ed in 2006.
In the last 3 years, num bers show ed a slight decrease. In the n o rth ­
w estern N o rth Sea, porpoise strandings w ere increasingly observed
since 1990, w ith a m axim um o f 77 strandings re ac h ed in 2006.
A long the south-w estern N o rth Sea coast, n u m b ers highly
increased from 2000 onw ards. In the n o rth -ea stern N o rth Sea,
strandings w ere increasingly re p o rte d since 1990, w ith m axim um
n u m b e r re co rd e d in 2005 (265 strandings). In the m id-eastern a n d
south-eastern N o rth Sea, averages o f 15 a n d 35 strandings .year 1
respectively w ere observed in the 1990’s. Since 2000, higher
n um bers w ere recorded. A long the eastern C hannel, less th a n 10
strandings .year- w ere observed until 2001.Since 2002, num bers
increased to 59 potpoises stran d ed in 2007. A ro u n d 10 potpoises
w ere found stran d ed in the w estern C h a n n el every y ear betw een
2 - H a r b o u r P o r p o i s e S tr a n d in g P a t t e r n s in N o r t h w e s t
E u r o p e a n W a te rs
Spatial patterns in observed harbour porpoise stranding
data. A total o f 10,038 stran d ed h a rb o u r porpoises w ere used
from across the w hole study a rea (figure 5): 2,534 in the n o rth ­
eastern N o rth Sea, 1,473 in the m id-eastern N o rth Sea, 2,745 in
the south-eastern N o rth Sea, 845 in the north-w estern N o rth Sea,
662 in south-w estern N o rth Sea, 289 in eastern C han nel, 878 in
w estern C h a n n el a n d 607 in the B ay o f Biscay, over the study
p erio d 1990-2009. T h e average frequency o f stranding events was
0.12 h a rb o u r porpoise stranded.km '.y e a r *, coastline being
m easured in straight line along the m ain orien tatio n o f the subareas.
T h e highest frequency o f stran d ed h a rb o u r porpoises was
observed along the south-eastern N o rth Sea coast, w here it
re ac h ed 0.4 strandings.km - '.y e a r - 1 . H ig h frequencies w ere
observed along the m id-eastern N o rth Sea w ith 0.28 strandings.km - '.y e a r-1 a n d 0.32 along the n o rth -ea stern N o rth Sea.
N orth-w estern parts o f the N o rth Sea a n d the C h a n n el show ed
low er frequencies w ith 0.09 strandings.km '.y e a r '. Finally the
lowest frequencies w ere found in the south-w estern N o rth Sea
(0.06 stranding.km '.y e a r '), in the Bay o f Biscay (0.05
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Stranding Anomaly as Population Indicator
Total
North W estern North Sea
North Eastern North Sea
South W estern North Sea
South Eastern North Sea
Mid-Eastern North Sea
W estern Channel
Eastern Channel
Bay o f Biscay
Figure 4. A verage m o n th ly d istrib ution o f observed strandings (black bars), expected strandings (grey bars) and stranding
ano m aly (w hite bars) (n) from 1 990 to 2009.
d o i:1 0 .1 3 7 1 /jo u rn a l.p o n e .0 0 6 2 1 8 0 .g 0 0 4
1990 a n d 1996, before increasing to a m ax im u m o f 151 strandings
in 2004. Since 2005, n u m b ers decreased. A long the Bay o f Biscay,
a n average o f 4 porpoises.year-1 was observed stran d ed from
1990-1996. F ro m 1997 on, n u m b ers increased to 101 reco rd ed in
2006 a n d low er n u m b ers w ere observed since th en (around 63
strandings .year *).
Seasonal patterns in observed harbour porpoise
stranding data. H a rb o u r porpoise stranding num bers w ere
sum m ed by m o n th to highlight seasonal distribution o f strandings
across the study area: as m an y as 53% o f porpoise strandings w ere
observed b etw een M a rch a n d Ju ly (figure 4). E xcept in n o rth ­
eastern N o rth Sea, highest num bers w ere observed betw een
M a rc h a n d M ay (twice h igher th a n du rin g the rest o f the year).
D u rin g spring or sum m er, high stranding num bers w ere recorded
in one m o n th . In the n o rth -eastern N o rth Sea, strandings recorded
in J u n e a n d Ju ly w ere 15 tim es higher th a n in w inter. T h e
coefficient o f variations was one o f the highest in the study a rea
(CIV = 0.94). In the C hannel, seasonal p attern s show ed highest
values from J a n u a ry to April. In w inter, the m axim um value was
observed in J a n u a ry in the w estern p a rt a n d decreased regularly
until J u n e , w hereas n u m b ers increased from J a n u a ry to A pril in
the eastern C hannel. A long the B ay o f Biscay coasts, highest
porpoise num bers w ere observed from J a n u a ry to A pril, a n d very
few w ere re co rd e d the rest o f the year. T h e high variations
betw een w inter a n d sum m er w ere confirm ed by the highest
coefficient o f v ariation (CIV = 0.96).
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3 - S t r a n d in g A n o m a li e s
Spatial comparisons. W e c o m p a red expected strandings.km _1.year_1 in the 8 large E u ro p e a n regions to observed
strandings .km '.y e a r 1 collected by stranding netw orks in these
subareas a n d found th a t difference was not statistically significant
(P= 0.480).
Long term trends. A t the E u ro p ea n scale, the difference
betw een observed a n d expected h a rb o u r porpoise strandings was
significant (iP = 0.021). T his result was found in all regions
(T V IO -3 in each case) except along the south-w estern a n d
north-w estern N o rth Sea coasts (P= 0.379 a n d 0.199, respectively)A t a E u ro p ea n scale, stranding ano m aly show ed a regular
increase a n d two breakpoints w ere d etected in 2001 a n d 2005
(figure 7). T ren d s in anom alies becam e positive after the first
break p o in t a n d a strong increase started w ith the second
breakpoint.
T h e Bay o f Biscay, the C hannel, the m id-eastern a n d the south­
eastern N o rth Sea show ed negative ano m aly from 1990 to 2000
th a t becam e positive thereafter. Since 2005, these anom alies
becam e strongly positive a n d show ing th a t there w ere m u ch m ore
porpoises observed stran d ed th a n expected u n d e r the null
hypothesis. A long the w estern C h a n n el coast, high positive
anom alies w ere observed d u rin g a short p e rio d from 2002 to
2005. Since 2005, these values becam e m ore regular a n d closer to
0. T h e north-w estern, n o rth -ea stern a n d south-w estern N o rth Sea
7
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Stranding Anomaly as Population Indicator
L egend
S tran d e d h a rb o u r p o rp o is e s (n)
I 11 -s
I
56°N
1 6 -1 0
I 111
l~ B 2 1
20
■
31
40
■
41
60
M
61
100
■
101 - 200
■
201 - 350
■
351 - 600
30
B athym etry (m)
-1500
-1000
-500
-100
46°N
46°N
Figure 5. H arb ou r porpoise strandings collected by European stranding schemes (n) fro m 1 990 to 2009.
d o i:1 0 .1 3 7 1 /jo u rn a l.p o n e .0 0 6 2 1 8 0 .g 0 0 5
coast show ed different profiles a n d anom alies w ere steadier over
the study period. O ccasional high stranding anom alies w ere
re co rd e d in those areas. T h e decrease in stranding anom alies
observed in recent years for several regions was n o t identified as a
break p o in t by the analysis, possibly because not e n ough years after
the a p p a re n t start o f this putative new tren d are available to date.
Seasonal patterns. C o rrelo g ram o f the stranding anom aly at
E u ro p ea n level show ed a slow decrease w ith tim e (figure 8). T h e
m ax im u m correlation was found at a tim e-lag o f 12 m onths,
reflecting a positive linear relationship betw een variables separated
by 1 year, highlighting the strong seasonal com p o n en t o f stranding
d ata. T h e sam e general p a tte rn was also observed along the south­
eastern a n d m id-eastern N o rth Sea coasts.
V ery slight trends w ere d etected in the C h an n el, as show n by
the autocorrelations always > 0 , irrespective o f tim e lag. N ever­
theless a strong seasonality was d etected w ith a 12-m onths period.
F u rth e rm o re , the Bay o f Biscay a n d n o rth -ea stern N o rth Sea
show ed a negative correlation focused on 6-m onths periodicity,
explained by a strong seasonal p a tte rn a n d the lack o f detectable
tre n d in the tim e series. Finally, the n orth-w estern a n d south­
w estern N o rth Sea coast did suggest neith er strong seasonal
p a tte rn n o r tren d , except a positive auto co rrelatio n a t lag 1 year,
suggesting a slight 12-m onths p a tte rn .
In the w hole study area, the m onthly decom position o f
stranding anom alies show ed th a t they w ere highest in A pril a n d
Ju ly , a n d lowest from S eptem ber to F eb ru ary (figure 4). A strong
seasonality was observed in b o th C h a n n el regions a n d in the Bay
o f Biscay, w ith positive anom alies in w inter a n d negative du rin g
the rest o f the year. T h e strongest seasonality was observed in
n o rth -eastern N o rth Sea, w ith high positive ano m aly calculated
from J u n e to August. In all o th er regions, this schem e was n o t so
strong. E ven if positive anom alies w ere still observed in late w inter
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a n d spring, they rem a in e d irregular, w ith irregular changes in
anom aly sign. T h e differences betw een observed a n d expected
stranding seasonality w ere significant in the w estern C han n el
(iP= 0.019), the B ay o f Biscay (iP = 0.019) a n d the north -eastern
N o rth Sea (P < 10—3). In eastern C h a n n el a n d in the rest o f the
N o rth Sea, these differences w ere n o t significant (P> 0.785).
D iscussion
1-G en e ra l
T his w ork is a n entirely novel a p p ro ac h to analysing a n d
in terp retin g small cetacean stranding d a ta th a t is a im ed a t taking
drift, the m ajor confounding factor involved in the stranding
process, into account w h en analysing stranding d a ta sets. Firstly
we constructed stranding tim e series expected u n d e r the assum p­
tion th a t d e ad small cetacean b e uniform ly distributed in tim e a n d
space a n d therefore th a t spatio-tem poral p attern s in stranding
frequency w ould entirely result from drift conditions. T h e
exposure to strandings on the coast o f 8 large E u ro p ea n subareas
was show n to vary b y a factor o f 1 to 7 d ep en d in g on the
orien tatio n o f the coast relative to prevailing w inds. Secondly,
expected small cetacean stranding tim e series a n d seasonal
p attern s w ere c o m p a red to observed h a rb o u r potpoise stranding
d a ta o n the assum ption th a t any deviation from the null hypothesis
w ould help disentangle the com plexity o f observed stranding
records a n d express their biological c om ponent, i.e. spatiotem poral p attern s in co m bined h a rb o u r porpoise density a n d
m ortality.
T w o im p o rta n t aspects o f this a p p ro ac h are its large spatial scale
(from the n o rth e rn N o rth Sea to the sou th ern Bay o f Biscay) a n d
long tem poral span (20 years). U n c erta in ty in carcasses drift
m odelling was estim ated at a few 10 s o f kilom etres [26], well
April 2013 I Volume 8 | Issue 4 | e62180
Stranding Anomaly as Population Indicator
Total
North W e ste rn North Sea
North E astern North Sea
s
%
s
s
s
s
s
1990
1995
2000
1990
2005
1995
2000
2005
1990
1995
2000
2005
year
S ou th W e stern North Sea
South E astern N orth S ea
M id-E a stern N orth Sea
s
s
s
s
s
s
1995
2000
E astern C hannel
W estern C hannel
1990
2005
2000
2005
2000
2005
B ay o f B iscay
s
s
s
s
s
s
s
§s2000
1990
1995
2000
1990
1995
year
Figure 6. Annual num bers o f observed harbo ur porpoise strandings (n) from 1 990 to 2009.
d o i:1 0 .1 3 7 1 /jo u rn a l.p o n e .0 0 6 2 1 8 0 .g 0 0 6
below the sizes o f study a re a a n d sub-areas sizes. In addition, the
size o f the study a rea encom passes a large p ro p o rtio n o f the
h a rb o u r poip o ise po p u latio n distribution in north-w estern E u ro p e
a n d a scale at w hich massive changes in distribution w ere show n
betw een 1994 a n d 2006 b y the SC A N S a n d SC A N S II surveys
[52,53]. F u rth e rm o re , genetic analyses suggested th a t h a rb o u r
porpoises from Bay o f Biscay to the N o rth Sea m ay constitute a
single continuous system u n d e r isolation b y distance [54], T h e
long d u ra tio n o f the analyses potentially allows changes in trends
to be differentiated from h igher frequency noise in stranding data.
T o cover this large geographical scope a n d tem poral span w e have
lu m p ed together d a ta sets from seven distinct n ational stranding
schem es. A lthough this is a n obvious strength o f the study, it also
introduces a source o f h eterogeneity th a t is difficult to assess as a
result o f the specific history a n d m an ag em en t o f each o f these
schem es a n d the levels a public aw areness o n these issues (with is
central in the rep o rtin g process) th a t have evolved at different rates
betw een countries (possibly also w ithin countries).
T h e d eterm in atio n o f 8 large subareas acco rd in g to coast-line
orientations ra th e r th a n E u ro p e a n bo u n d aries sm oothed stranding
p attern s collected at c o untry scale, b u t is considered to be m uch
m ore relevant o n a n ecological p o in t o f view th a n statistics
analysed o n a n ational basis. N evertheless, increased porpoise
strandings observed since 2000 along the D u tch , B elgian a n d
PLOS ONE I www.plosone.org
n o rth e rn F re n c h coasts [55,56] are consistent w ith changes
detected in the regions created for the presen t study. Increased
strandings along w estern N o rth Sea a n d C h a n n el w ere also
consistent w ith trends in stranding num bers collected along ETK
coasts since late 1990’s [38], Seasonal p attern s in stranding d a ta
analysis carried out a t n ational level m ay b e slightly different to the
p attern s observed in the presen t work, b u t the p re d o m in an t
seasonality w ith m ax im a in w inter m onths re m a in e d strong in
eastern N o rth Sea, C h a n n el a n d B ay o f Biscay [38,56], B oth
stranding m ax im a re ac h ed in M a rc h a n d A ugust along Belgian
a n d D u tc h coasts w ere identified in o u r south-eastern N o rth Sea
a rea [55]. T h e strong seasonality focused on sum m er m onths
d escribed along the n o rth -eastern N o rth Sea coasts w ere consistent
w ith G e rm an stranding d a ta [30].
T h e m ain tool used in this study was the drift pred ictio n m odel
M O T H Y . M O T H Y characteristics im posed a lim itation to the
n u m b e r o f theoretical cetaceans (238) w hich drift could be
m odelled at any single date a n d therefore con strain ed the
resolution o f the grid to 0.75" in latitu d e a n d longitude. G iven
the resolutions used to m odel distributions o f top m arine
pred ato rs, th eir p re y a n d h u m a n activities (e.g. IC E S statistical
grid cells) the resolution o f the presen t w ork is largely consistent
w ith m ost o th er relevant source o f inform ation. A n o th er constraint
9
April 2013 I Volume 8 | Issue 4 | e62180
Stranding Anomaly as Population Indicator
Total
North Western North Sea
North Eastern North Sea
§
1990
1995
2000
2005
2010
1990
1995
2000
2005
2010
1990
1995
2005
2010
Mid-Eastern North Sea
South Eastern North Sea
South Western North Sea
2000
Year
Year
o
1990
1995
2000
2005
2010
1990
1995
1995
2005
2010
2000
2005
2010
1990
1995
Year
1990
1995
2000
2005
2010
Year
Eastern Channel
Western Channel
1990
2000
Year
Year
Bay of Biscay
2000
Year
2005
2010
1990
1995
2000
2005
2010
Year
Figure 7. Long term harbo ur porpoise stranding anom alies in large subareas (n) from 1 990 to 2 0 0 9. Black a rro w s re p r e s e n t d e te c te d
b re a k p o in ts in tim e series.
d o i:1 0 .1 3 7 1 /jo u rn a l.p o n e .0 0 6 2 1 8 0 .g 0 0 7
o f M O T H Y relates to its geographical extent a n d justifies w hy
Spanish a n d Irish d a ta can n o t b e added.
T h e null hypothesis is used in ecology to construct a situation
w here n o th in g h appens a n d to test the effect o f several controlled
p a ram ete rs [57]. T h is hypothesis is used to disentangle the p a rt o f
process a p p ea red at ra n d o m [58]. In ecology, one exam ple am o n g
others was to use it to construct theoretical fish com m unities a n d
test one by one several p a ram ete rs [59]. T his w ork is the first
a tte m p t to use a sim ilar a p p ro ac h in the analysis o f cetacean
stranding data, in the aim o f disentangling biological processes
from drift-related processes.
from these cells to re ac h a coast w ithin 30 days. U n d e rstan d in g
how the p robability o f stranding varies seasonally a n d spatially is
essential to appreciate the geographical representativeness o f d a ta
collected from stran d ed cetaceans. H e re, highest probabilities to
get stran d ed a p p e a r close to the coasts in the sum m er a n d extend
over the shelf in the w inter.
Seasonal w ind clim atology explains the seasonality in stranding
probability a n d expected strandings b u t only partially drives
seasonal stranding pattern s. Sim ilar p attern s w ere found along the
Bay o f Biscay a n d the C h a n n el coasts w ith m ax im a expected in
w inter a n d m in im a in sum m er, b u t the am plitude o f the seasonal
p attern s was m u ch larger in observed stranding d a ta th a n in
expected stranding d ata. O pposite p attern s are observed betw een
w estern (m axim a in M ay) a n d eastern (m inim a in A pril-M ay) coast
o f the N o rth Sea. In north-w estern E urope, strongest w ind systems
are observed in w inter, from O c to b er to F e b ru a ry [60,61], M ain
w ind orien tatio n is from the north-w est in the Bay o f Biscay a n d
w est-south-w est in the C h a n n el a n d the N o rth Sea [60,61],
2-Drift C o n d i t i o n s in E u r o p e
T h e m onthly clim atology o f stranding p robabilities in E u ro p ea n
w aters show ed a clear seasonal p a tte rn as a result o f the strong
difference observed b etw een w inter a n d sum m er drift conditions.
Cells located in coastal areas p rovided strandings y ear ro u n d , as
exem plified in the C hannel. C onversely, cells located further
offshore in the Bay o f Biscay a n d in the w estern central N o rth Sea
could seasonally be too far aw ay to allow any carcass originating
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April 2013 I Volume 8 | Issue 4 | e62180
Stranding Anomaly as Population Indicator
Total
North W estern North S ea
I i i
o.o
o
0.5
1.0
1.5
TP~
2.0
South W estern North S ea
North Eastern North Sea
11111 I
Lag (year)
South Eastern North Sea
Mid Eastern North S ea
dCO
<o
o
d
o
o
o
0.0
0.5
1.0
1.5
Eastern Channel
W estern Channel
III
2.0
Bay of Biscay
_i_L
0.0
0.5
1.0
1.5
2.0
0.0
0.5
1.0
1.5
2.0
Figure 8. Correlogram s of h arbour porpoise stranding anom aly in large subareas from 1990 to 20 0 9. If autocorrelation falls outside the
dotted lines, it is considered to be significant 0 at a 5% probability level.
doi:10.1371/journal.pone.0062180.g008
w estern N o rth Sea, a slight seasonal p a tte rn was described, b u t no
tre n d was d etected in stranding anom aly.
T hese results suggested th a t d e a d h a rb o u r porpoise num bers
increased since 1990 a n d w ere observed du rin g the w hole year.
T hese results w ere consistent w ith several previous studies based
on at-sea sighting analysis, suggesting th a t h a rb o u r porpoises w ere
observed y e ar-ro u n d a n d increased in the p ast 10 years m ostly in
N o rth Sea [30,62-65]. T h e seasonality d etected in north -eastern
N o rth Sea can b e explained by a seasonal m ovem ents a n d an
increase o f porpoise a b u n d an c e along these coasts. D ed icated
surveys show ed an increase o f porpoise e n co u n ter ra te in sum m er
along G e rm an a n d D anish coasts [30,47]. A dditionally, sum m er is
the poipoise calving p e rio d a n d calves o ccurrence rem ain high in
stran d ed porpoise tim e series [30,47]. In the Bay o f Biscay a n d
w estern C hannel, seasonality was the p re d o m in an t signal. O nly
w inter m axim a increased since 2000, w hereas the difference was
always negative in the sum m er for the w hole 20 years long study
period. T his could be explained b y a change in h a rb o u r porpoise
distribution in the sum m er. T h e use o f platform -of-opportunity
d a ta collected m ostly in the sum m er show ed th a t porpoises are
3 - l n t e r p r e t a t i o n o f H a r b o u r P o r p o i s e S tr a n d in g T im e
Series
Positive (is. negative) standing anom alies suggested th at
observed stranding n u m b ers w ere higher (is. lower) th a n expected.
In o th er w ords, dep artu res from predictions m ad e u n d e r the null
hypothesis (uniform ity o f distribution in space a n d time) reveal the
spatio-tem poral p attern s o f the biological com ponents o f h a rb o u r
porpoise stranding records.
W ith the exception o f the w estern N o rth Sea, long term
stranding anom alies w ere always significantly different from 0,
indicating th a t drift alone c an n o t explain inter a n d in tra -an n u a l
variations in h a rb o u r porpoise stranding frequency. O n average,
expected m in im a a n d m ax im a ra n g ed from 1 to 3, w hereas
observed num bers ran g ed from 1 to 10 a n d stranding anom alies
ra n g ed from 1 to 500. Seasonality analyses (correlogram s a n d
W ilcoxon tests) show ed th a t in the B ay o f Biscay a n d w estern
C hannel, the seasonal p a tte rn was p re d o m in an t a n d did not
explain by drift conditions. In eastern C h a n n el a n d south to m ideastern N o rth Sea, the long term trends was p re d o m in an t a n d the
seasonal signal was partially explained by drift conditions. In
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April 2013 I Volume 8 | Issue 4 | e62180
Stranding Anomaly as Population Indicator
observed in the w estern C h a n n el a n d very few sightings are
re co rd e d in the Bay o f Biscay p ro p e r [66,67].
Finally, south-w estern a n d north-w estern N o rth Sea coasts
presen ted m o re sim ilarity w ith the null hypothesis th a n a n y o th er
region in the study area. O bserved a n d expected tim e series w ere
n o t significandy different a n d this difference is quite random ly
distributed a ro u n d 0 across the study period. In all o th er regions,
observed porpoise strandings w ere low er th a n expected u n d e r the
null hypothesis before 2000 a n d higher thereafter. T h is w ould
suggest th a t h a rb o u r porpoises w ere n o t uniform ly distributed in
tim e a n d space in E u ro p ea n w aters since 1990, except along the
w estern N o rth Sea coasts. In o th er w ords changes occu rred in
a b u n d an c e a n d /o r m ortality o f h a rb o u r porpoises in n o rth ­
w estern E u ro p ea n w aters. T his conclusion was consistent w ith the
hypothesis suggested after the SC A N S a n d SC A N S -II surveys
carried o u t in 1994 a n d 2005 [52,53]. T hese surveys suggested a
southern shift in the h a rb o u r porpoise distribution ra th e r th a n a
change in their a b u n d an c e. T h e difference in tim e series
calculated in the study a re a suggested a n increase o f d e ad
porpoises since 2000. T h e change in the sign o f stranding
anom alies could b e due to a change in a b u n d an c e o f d e ad
porpoises in o u r calculation area.
In 1994 (at the tim e o f the first SC A N S survey) a b u n d an c e a n d
m ortality o f porpoises in n o rth e rn N o rth Sea (west a n d east)
seem ed to be fairly stable a n d close to the null hypothesis a n d w ere
low er in the rest o f study area, as suggested by generally negative
stranding anom alies in all regions except n o rth e rn N o rth Sea.
T hese results w ere in line w ith SC A N S results, w ith highest
densities o f porpoises observed in the n o rth e rn N o rth Sea [52].
Since 2000, increasing d e a d porpoise n u m b ers (increasing
stranding anom alies) w ere observed first in the south-eastern a n d
south-w estern N o rth Sea, th en in the w estern C hannel, the south­
eastern a n d m id-eastern N o rth Sea, the Bay o f Biscay a n d finally
the eastern C h a n n el as show n by b re ak p o in t analysis. In 2005
(second SC A N S survey), high stranding anom alies w ere observed
in B ay o f Biscay, w estern C h a n n el a n d all areas o f the eastern
N o rth Sea, w hereas low er n u m b ers w ere observed in the eastern
C h a n n el a n d the south-w estern N o rth Sea. S tran d in g anom alies
highlighted changes in porpoise a b u n d an c e a n d /o r m ortality.
Increases o f these anom alies can suggest either a n increase in
porpoise a b u n d an c e in the a re a o r an increase in m ortality rate.
T h e p a tte rn in stranding ano m aly d etected gradually du rin g the
2000’s along the N o rth Sea, the C h a n n el a n d the B ay o f Biscay
w ould be m ore consistent w ith a m ovem ent o f the population.
T h erefo re stranding ano m aly increases could b e explained b y an
increase o f porpoises a t sea in these areas. T hese results w ere very
consistent w ith SC A N S II results, even if no h a rb o u r porpoises
w ere observed in the Bay o f Biscay d u rin g this survey [53]. T his
can b e explained b y the low e n co u n ter ra te observed in sum m er in
the Bay o f Biscay [66,67]; p ro b ab ly due to a strong seasonal
p a tte rn in distribution o r h a b ita t use in the Bay o f Biscay.
M oreover the efficiency im p ro v em en t o f stranding netw orks in
som e areas in the early 1990’s w ould suggest th a t changes in
stranding ano m aly w ould p ro b ab ly n o t be w holly biological in
origin. N evertheless, the m agnitude o f increase c an n o t be entirely
explained by changes in re p o rtin g effort because m ost E u ro p ea n
stranding netw orks operate efficiendy since decades.
Increase in h a rb o u r porpoise stranding ano m aly o ccurring
earlier in the w estern C h a n n el th a n in the eastern C h a n n el w ould
suggest th a t the southw ard m ovem ent o f anim als w ould have
occu rred along b o th sides o f the British Isles.
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4 - S t r a n d in g s a s a M o n i to ri n g Tool
T h e com parison a n d the relevance o f results o b tain e d in this
study c o m p a red to sighting surveys c o n d u cted in the N o rth Sea
a n d a d ja ce n t w aters considerably im proves the interest o f using
strandings as a m on ito rin g tool. T h e analysis o f stranding
anom alies ra th e r th a n raw d a ta cleared the stranding signal from
the effect o f drift conditions. T h e link b etw een strandings a n d
cetacean a t sea becam e clearer a n d sim plified the u n d e rstan d in g o f
stranding tim e series. D ed icated surveys p rovided snap-shot
pictures o f small cetacean distribution a n d absolute a b u n d an c e
a t decadal interval. T h e m on ito rin g o f strandings a n d the analysis
o f stranding anom alies w ould provide continuous distribution a n d
relative a b u n d an c e inform ation, cleared from biases related to
variations in drift condition. T h e im p ro v em en t o f the know ledge
o f the relationship b etw een strandings a n d cetaceans a t sea
constitutes a m ajo r step in the use o f strandings as indicators o f atsea populations. M o n ito rin g stranding d a ta could provide m aps o f
the likely origin o f porpoises a t sea, to identify high m ortality areas
a n d incidences w ith h u m a n activities [26]. S tra n d in g d a ta will
never provide a b u n d an c e estim ates, b u t the cost o f dedicated
surveys a t E u ro p ea n scale is too high to provide cetacean
m on ito rin g d ata. T h e com b in ed use o f b o th tools w ould be
relevant in the developm ent o f a n efficient m on ito rin g strategy,
notably in context o f the C onservation P lan for h a rb o u r porpoises
in the N o rth Sea, carried o u t b y A S C O B A N S.
Finally, the use o f stranding anom aly as a n ind icato r o f cetacean
m ortality could becom e a n ad ditional efficient tool for environ­
m ental w atch a n d to detect variations in strandings acco rd in g to
changes o f a b u n d an c e o r m ortality o f cetaceans a t sea. F o r the first
tim e, the integration o f E u ro p ea n d a ta will allow to look at
biological p h e n o m e n o n ra th e r th a n natio n al variations. C ause o f
d e ath could b e identified b y carcass exam ination a n d stranding
anom alies could be calculated for each cause o f d eath. It w ould
provide relevant in form ation o n spatial a n d tem poral variations in
d e ath causes, im prove the efficiency o f stranding m on ito rin g a n d
allow early decision m aking in case o f unusual m ortality events.
5 -C o n c lu s io n
It is com m only a d m itted th a t stranding schem es provide lowcost indicators a n d yield reasonable d a ta o n the frequency o f
occurrence o f species in the regions they cover [23,24,68]. T hus,
strandings provide sim ilar ran k -o rd er relative abu n d an ces as live
surveys [23,24], C onsequendy, stranding d a ta could provide
relevant low-cost inform ation on m ortality areas a t sea [26],
relative densities, distribution, specific richness a n d num bers
c leared from drift variations as well. T his study constitutes a
significant im p ro v em en t in stranding d a ta statistical credibility in
the c ontext o f m on ito rin g pop u latio n a n d p roviding w orldw ide
indicators for cetaceans a n d m ore widely for m arin e m egafauna
like sea turtles o r seabirds. T h e construction o f new indicators for
wildlife m on ito rin g strategies is still a n issue o f m ajo r concern in
conservation biology, in p a rticu la r in the context o f the ever
increasing n u m b e r o f p roposed M a rin e P rotected A reas.
A ck n ow led gm en ts
T h e a u th o rs w ou ld like to th a n k all persons involved in th e different
n a tio n a l stra n d in g netw orks w h ic h p ro v id e d d a ta series fo r this w ork.
- P E LA G IS O b se rv a to ry thanks all m e m b e rs o f th e F re n c h stra n d in g
ne tw o rk fo r th e ir c o n tin u o u s effort in collecting stra n d in g d a ta . PE LA G IS
O b se rv a to ry is fu n d e d b y Ministère de IEcologie, du Développement Durable et de
IEnergie, a n d b y Communauté dAgglomération de la Ville de La Rochelle, w ith
s u p p o rt o f Région Poitou-Charentes a n d th e E u ro p e a n U n io n . T h e P h D thesis
o f Ft. P eltier w as s u p p o rte d b y th e Centre .National de la Recherche Scientifique
a n d b y Region Poitou-Charentes.
12
April 2013 I Volume 8 | Issue 4 | e62180
Stranding Anomaly as Population Indicator
- T h e U K C e ta c e a n S tran d in g s In v estig atio n P ro g ra m m e is fu n d e d by
D e fra in E n g la n d a n d th e D ev o lv ed A d m in istratio n s in S co tlan d a n d
W ales.
-T h e B elgian stran d in g s in te rv e n tio n n e tw o rk is s u p p o rte d b y th e R oyal
B elgian In stitu te o f N a tu ra l Sciences a n d b y th e B elgian Science Policy
- D a ta fro m S chlesw ig-H olstein, G e rm a n y w ere co llected p a rtly fu n d e d
b y th e G e rm a n F e d e ra l M in istry fo r th e E n v iro n m e n t, N a tu re C o n se rv a ­
tio n a n d N u c le a r Safety, th e G e rm a n F e d e ra l M in istry fo r E d u c a tio n a n d
R e se a rc h a n d th e M in istry o f E n v iro n m e n t, N a tu re C o n se rv a tio n a n d
A g ricu ltu re o f Schlesw ig-H olstein. W e w o u ld like to th a n k M a rio n
R a d e m a k e r a n d D r. A n d re a s R u se r fo r th e d a ta h a n d lin g a n d all involved
perso n s fo r th e collection o f d a ta . D a ta fro m L o w er-S ax o ny, G e rm a n y
w e re e x tra c te d fro m a d a ta b a s e o f s tra n d e d a n im als, h e ld a t the
N a tio n a lp a rk A d m in istra tio n W a d d e n Sea o f L o w e r Saxony, W ilh elm ­
shaven.
- T h a n k s to the D a n ish N a tu re A gency for p ro v id in g s tra n d in g d a ta in
D a n ish w aters.
Author C ontributions
C o n ce iv e d a n d d e signed the e xperim ents: H P V R . A nalyzed the d ata: H P .
C o n trib u te d re a g e n ts/m a te ria ls /a n a ly s is tools: H JB K C JC R C W D P D
R D J H T J LFJ P D J G O K U S O V C . W ro te th e p a p e r: H P P D J V R .
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ecosystem s. In : C a m p h u s e n C J, B o y d IL , W a n le ss S, ed ito rs. T o p P re d a to rs in
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