FIELD EXPERIMENTS SHOW THAT ACOUSTICPINGERS REDUCE MARINE MAMMAL BYCATCHIN THE CALIFORNIA DRIFT GILL NET FISHERY
JAY BARLOW
GRANT A. CAMERON1
Southwest Fisheries Science Center,National Marine Fisheries Service,
8604 La Jolla Shores Drive, La Jolla, California 92037, U.S.A.E-mail: [email protected]
ABSTRACT
A controlled experiment was carried out in 1996–1997 to determine whetheracoustic deterrent devices (pingers) reduce marine mammal bycatch in theCalifornia drift gill net fishery for swordfish and sharks. Using Fisher’s exact test,bycatch rates with pingers were significantly less for all cetacean species combined(P , 0.001) and for all pinniped species combined (P ¼ 0.003). For species testedseparately with this test, bycatch reduction was statistically significant for short-beaked common dolphins (P ¼ 0.001) and California sea lions (P ¼ 0.02). Bycatchreduction is not statistically significant for the other species tested separately, butsample sizes and statistical power were low, and bycatch rates were lower inpingered nets for six of the eight other cetacean and pinniped species. A log-linearmodel relating the mean rate of entanglement to the number of pingers deployedwas fit to the data for three groups: short-beaked common dolphins, other cetaceans,and pinnipeds. For a net with 40 pingers, the models predict approximately a 12-fold decrease in entanglement for short-beaked common dolphins, a 4-fold decreasefor other cetaceans, and a 3-fold decrease for pinnipeds. No other variables werefound that could explain this effect. The pinger experiment ended when regulationswere enacted to make pingers mandatory in this fishery.
Key words: bycatch, fishery, pinger, cetacean, dolphin, pinniped, Delphinus delphis,Zalophus californianus, short-beaked common dolphin, California sea lion.
Acoustic deterrent devices (pingers) reduced the bycatch of harbor porpoise(Phocoena phocoena) in bottom-set gill nets during controlled experiments: in theGulf of Maine (Kraus et al. 1997), in the Bay of Fundy (Trippel et al. 1999), alongthe Olympic Peninsula (Gearin et al. 2000), and in the North Sea.2 In all cases
1 Current address: Scripps Institution of Oceanography, UCSD, 9500 Gilman Drive, La Jolla,California 92093, U.S.A.
2 Larsen, F. 1997. Effekten af akustiske alarmer pa bifangst af marsvin i garn. Report number 44-97(unpublished). Available from the Danish Institute for Fisheries Research, Jægersborgvej 64-66,DK-2800 Kgs. Lyngby, Denmark.
265
MARINE MAMMAL SCIENCE, 19(2):265–283 (April 2003)� 2003 by the Society for Marine Mammalogy
a large (approximately 77%–90%) decrease in harbor porpoise mortality wasachieved in short-term experiments. The mechanisms are not well understood(Kraus et al. 1997), but in field trials and in captive studies, the sounds produced bypingers appear to be aversive to harbor porpoises (Kastelein et al. 1995, 2000; Laakeet al.;3 Culik et al. 2001). Another pinger experiment was conducted in 1994 ona drift gill net fishery for swordfish along the U.S. east coast whose bycatchincluded a wide variety of cetaceans. Results of that experiment were somewhatequivocal: in paired tests pingered nets had lower bycatch, but both pingered andunpingered nets in the experiment had higher bycatch than unpingered nets in therest of the fleet.4 Prior to these recent successes, the use of active or passive acousticdeterrents showed little or no effect on net entanglement of Dall’s porpoises(Phocoenoides dalli) (Hatakeyama et al. 1994), and there was little optimism in thescientific community that such approaches would work with other species (Dawson1994, Perrin et al. 1994, Jefferson and Curry 1996). The recent success of pingers inreducing harbor porpoise entanglements in bottom set gill nets prompted a re-evaluation of their potential to reduce mortality of other cetacean species in otherfisheries.5 In this paper we describe an experiment to evaluate the effectiveness ofpingers to reduce cetacean mortality in the drift gill net fishery for swordfish andsharks along the coasts of California and Oregon.
This drift gill net fishery typically operates 37–370 km offshore from southernCalifornia to northern California and, in some years, to Oregon (Fig. 1). Theprimary season for broadbill swordfish (Xiphias gladius) is between 15 August and31 January, but some vessels fish for sharks (primarily common thresher, Alopiusvulpinas, and shortfin mako, Isurus oxyrinchus) between 15 May and 15 August.There were approximately 130 vessels actively fishing in 1995.6 Vessels aretypically 9–23 m in length, and each vessel fishes at night with one multifilamentgill net (stretched mesh size of 43–56 cm) with a maximum length of 1,830 m.Nets are suspended completely below the surface by float lines which werea minimum of 11 m in length. Previous bycatch included a wide assortment ofcetacean species (Julian and Beeson 1998) including delphinids (common dolphins,Pacific white-sided dolphins, northern right whale dolphins, Risso’s dolphins, pilotwhales, bottlenose dolphins, and killer whales), beaked whales (Cuvier’s beakedwhales, Baird’s beaked whales, and Mesoplodon spp.), dwarf sperm whales, spermwhales, and humpback whales (see Table 2 for scientific names). Based on the
3 Laake, J., D. Rugh and L. Baraff. 1998. Observations of harbor porpoise in the vicinity of acousticalarms on a set gill net. U.S. Department of Commerce, NOAA Technical Memorandum NMFS-AFSC-84 (unpublished). 40 pp. Available from the National Marine Mammal Laboratory, 7600 Sand PointWay NE, Seattle, WA 98115, U.S.A.
4 DeAlteris, J., E. Williams and K. Castro. 1994. Results of an experiment using acoustic devices toreduce the incidental take of marine mammals in the swordfish drift gillnet fishery in the NorthwestAtlantic Ocean. Unpublished report. 10 pp. Available from the University of Rhode Island, Kingston,RI 02881, U.S.A.
5 Reeves, R. R., R. J. Hofman, G. K. Silber and D. Wilkinson. 1996. Acoustic deterrence of harmfulmarine mammal-fishery interactions. Proceedings of a workshop held in Seattle, Washington, 20–22March 1996. U.S. Department of Commerce, NOAA Technical Memorandum NMFS-OPR-10(unpublished). 70 pp. Available from the NMFS Office of Protected Resources, 1335 East/WestHighway, Silver Springs, MD 20910, U.S.A.
6 Barlow, J., K. A. Forney, P. S. Hill, R. L. Brownell, Jr., J. V. Carretta, D. P. DeMaster, F. Julian, M.S. Lowry, T. Ragen and R. R. Reeves. 1997. U.S. Pacific Marine Mammal Stock Assessments: 1996.NOAA Technical Memorandum NOAA-TM-NMFS-SWFSC-248. 223 pp.
266 MARINE MAMMAL SCIENCE, VOL. 19, NO. 2, 2003
management scheme used in the United States, the estimated bycatch in 1992–1996 exceeded the PBR (Potential Biological Removal) for some marine mammalspecies and may not be sustainable.6 Concern about these bycatch levels promptedthe formation of the Pacific Offshore Cetacean Take Reduction Team to identifypotential solutions to this problem. The experiment described here was amongtheir first recommendations.
METHODS
Experimental Design
The experiment was designed to maximize statistical power and minimize bias.Each set was assigned randomly as either an experimental set (with pingers) ora control set (without pingers). The experiment was carried out only on those 20%–25% of fishing trips that carried National Marine Fisheries Service bycatchobservers. Prior to a trip, observers were given packets of 10 sealed and numberedenvelopes. Prior to each set, observers would open the envelope with the numbercorresponding to the sequential set number for that trip and would read a cardwhich would indicate whether that set was to be ‘‘experimental’’ or ‘‘control.’’Randomized within each packet of ten envelopes were five cards labeled ‘‘pingers’’and five labeled ‘‘no pingers.’’ If the number of sets per trip exceeded 10, a newpacket of envelopes was used starting with set number 11. To minimize thepotential for experimental manipulation, the selection of experimental and controlsets was made after the skipper had identified a fishing location and immediatelyprior to setting the net. A double-blind experimental design (such as that used byKraus et al. 1997 and Larsen2) was logistically infeasible.
Figure 1. Geographic distribution of sets with pingers (left) and without pingers (right)that were included in analyses.
267BARLOW AND CAMERON: PINGERS REDUCE BYCATCH
Dukane NetMark 10007 pingers were used during this experiment. Thesecommercially produced pingers emit a tonal signal of 300 msec duration every 4 secwith a fundamental frequency of 10–12 kHz and with significant harmonics up to100 kHz. The manufacturer cites a source level of 132 dB (re: 1 lPa @ 1 m), butindependent calibration studies have shown considerable variation in source levelsbetween 120 and 146 dB (X ¼ 138 dB, n ¼ 35).8,9 At a source level of 132 dB,these pingers were estimated to be 15 dB above ambient noise levels at 100 mdistance in the near-bottom environment in the Gulf of Maine (Kraus et al. 1997).Fishermen were instructed to place one pinger at each end of the floatline and at91 m intervals along the floatline and one pinger every 91 m along the leadlineoffset midway between the pingers on the floatline. A typical net of 1,830 m wouldtherefore require 21 pingers along the floatline and 20 pingers along the leadline.The actual number and configuration of pingers varied due to differences in netlength, pinger failures, and other uncontrolled factors (see below).
The experiment started at the beginning of the swordfish season in August 1996and continued until the end of October 1997 when pingers became mandatory inthis fishery. Based on previously measured rates of cetacean entanglement in thisfishery, an a priori power analysis10 indicated that approximately 1,100 sets wouldbe needed (550 with pingers and 550 without) to obtain a 90% probability ofdetecting a 50% decline in overall cetacean mortality (based on a Fisher exact testwith a ¼ 0.10, 1-tailed). A multiyear experiment was anticipated, but with only420 observed sets in 1996, the overall change in cetacean entanglement (a 77%reduction) was statistically significant.11 Based on these preliminary results, pingerswere made mandatory on 28 October 1997 via Federal regulations under theauthority of the U.S. Marine Mammal Protection Act, effectively ending thecontrolled experiment.
Data Collection
Observers on fishing vessels collected data on net specification (includingnumber of pingers used), environmental conditions at the beginning and end of theset, vessel activities during the set, and location at the beginning of the set (Table1). During net retrieval, the observer was stationed in a good position to observethe retrieval and recorded numbers and species of marine mammals (Table 2), seabirds, turtles, and fish caught. Data were checked by observers in the field and whenthey entered their data using a range-checking data entry program. Computer fileswere also checked for outliers, missing fields, and inconsistencies using an edit
7 The use of brand names does not imply endorsement by the National Marine Fisheries Service.8 Unpublished data from K. C. Baldwin, C. Pacheco, and S. D. Kraus, Center for Ocean
Engineering, University of New Hampshire, Durham, NH 03824, U.S.A.9 Unpublished data from D. Norris, Biomon, 718 C West Victoria Street, Santa Barbara, CA 93101,
U.S.A.10 Barlow, J. 1996. Design of an experiment to test the effectiveness of ‘‘pingers’’ to reduce marine
mammal by-catch in the west-coast drift gillnet fishery for swordfish and sharks. Unpublished report. 8pp. Available from the Southwest Fisheries Science Center, 8604 La Jolla Shores Drive, La Jolla, CA92037, U.S.A.
11 Julian, F. 1997. Cetacean mortality in California gill net fisheries: preliminary estimates for 1996.Paper SC/49/SM2 (unpublished). 13 pp. Available from the International Whaling Commission, TheRed House, Station Road, Histon, Cambridge CB4 4NP, United Kingdom.
268 MARINE MAMMAL SCIENCE, VOL. 19, NO. 2, 2003
Table1.
Des
crip
tion
sof
vari
able
suse
din
anal
yses
.V
aria
ble
types
coded
:ca
t¼
cate
gor
ical
,cn
t¼
con
tin
uou
s,or
d¼
ord
inal
,in
v¼
inte
rval
.R
ange
ofco
nti
nuou
sva
riab
leor
cate
gor
ies
ofca
tegor
ical
vari
able
giv
enunder
‘‘Val
ues
.’’M
ean
stat
isti
csco
nsi
stof
arit
hm
etic
mea
nfo
rco
nti
nuou
san
din
terv
alva
riab
les
and
odds
of‘‘1
’’fo
rbin
ary
cate
gor
ical
vari
able
s.‘‘3
’’in
dic
ates
test
sper
form
edon
each
vari
able
.‘‘E
nta
ngle
’’in
dic
ates
Wil
coxo
nte
sts
ofva
riab
lefo
rdif
fere
nce
inen
tangle
men
tra
te.‘
‘Pin
gs’’i
ndic
ates
Wil
coxo
nte
stfo
rdif
fere
nce
sin
vari
able
bet
wee
nse
tsw
ith
and
wit
hou
tpin
ger
s(c
hec
kon
random
izat
ion).
‘‘GLM
’’in
dic
ate
vari
able
incl
uded
inth
eG
ener
aliz
edLin
ear
Mod
elan
alys
es.
Mea
nst
atis
tics
Tes
ts
Var
iab
len
ame
Des
crip
tion
Typ
eV
alu
esA
llse
tsW
ith
pin
ger
sW
ith
out
pin
ger
sE
nta
ng
leP
ing
sG
LM
Controllable
mechanical
variables
dli
gh
td
eck
lig
hts
onat
nig
ht?
(1¼
on)
ord
f0,
1g
0.7
40
.75
0.7
63
33
eng
ine
eng
ine
onat
nig
ht?
(1¼
on)
ord
f0,
1g
0.0
80
.04
0.1
23
33
gen
erg
ener
ator
onat
nig
ht?
(1¼
on)
ord
f0,
1g
0.8
30
.83
0.8
23
33
stic
ks
nu
mb
erof
lig
ht
stic
ks
dep
loye
dcn
t[0
,4
0]
4.9
4.4
5.4
33
stic
ks
pre
sen
tli
gh
tst
ick
sd
eplo
yed
?(1
¼d
eplo
yed
)or
df0
,1g
0.4
20
.38
0.4
63
33
pin
gs
nu
mb
erof
pin
ger
sd
eplo
yed
cnt
[0,
45
]1
73
20
3
pin
gs
pre
sen
tp
ing
ers
dep
loye
d?
(1¼
dep
loye
d)
ord
f0,
1g
0.4
81
.00
.03
3
soak
nu
mb
erof
hou
rsn
etsu
bm
erg
edcn
t[0
,6
2]
12
.51
2.7
12
.33
3
soak
lo/h
i0¼
(soa
k<
12
h)
ord
f0,
1g
0.5
10
.53
0.4
83
33
1¼
(soa
k.
12
h)
son
arso
nar
onat
nig
ht?
(1¼
on)
ord
f0,
1g
0.1
40
.13
0.1
53
33
269BARLOW AND CAMERON: PINGERS REDUCE BYCATCH
Table1.
Con
tin
ued
.
Mea
nst
atis
tics
Tes
ts
Var
iab
len
ame
Des
crip
tion
Typ
eV
alu
esA
llse
tsW
ith
pin
ger
sW
ith
out
pin
ger
sE
nta
ngle
Pin
gs
GL
M
Environmentvariables
bcl
dcl
oud
cove
rat
star
tof
set:
inv
f0,
1,...
,9g
3.7
33
.61
3.8
53
lin
ear
scal
e0¼
0%
,8¼
10
0%
,9¼
too
dar
kb
cld
lo/h
i0¼
clea
r(b
cld,
5)
ord
f0,
1g
0.3
60
.35
0.3
63
33
1¼
clou
dy
(bcl
d>
5)
ecld
clou
dco
ver
aten
dof
set:
inv
f0,...
,9g
5.2
5.1
5.3
3li
nea
rsc
ale
0¼
0%
,8¼
10
0%
,9¼
too
dar
kec
ldlo
/hi
0¼
clea
r(e
cld,
5)
ord
f0,
1g
0.3
00
.31
0.3
03
33
1¼
clou
dy
(ecl
d>
5)
bb
eau
lo/h
iB
eau
fort
sea
stat
eat
star
tof
set
ord
f0,
1g
0.4
90
.49
0.4
83
33
0¼
calm
(,3
),1¼
rou
gh
(>3
)eb
eau
lo/h
iB
eau
fort
sea
stat
eat
end
ofse
tor
df0
,1g
0.4
40
.45
0.4
33
33
0¼
calm
(,3
),1¼
rou
gh
(>3
)se
ason
0¼
May
–O
ct,
1¼
Nov
–A
pr
cat
f0,
1g
0.5
60
.55
0.5
63
33
dep
thW
ater
dep
that
tim
eof
net
retr
ieva
l(f
ath
oms)
cnt
[0,
2,7
00
]1
,15
01
,16
71
,13
53
3
dep
thlo
/hi
0¼
shal
low
(,1
,00
0fa
thom
s)or
df0
,1g
0.4
60
.48
0.4
43
33
1¼
dee
p(.
1,0
00
fath
oms)
Net
variables
exte
nd
lo/h
i0¼
(ext
end,
37
ft)
cat
f0,
1g
0.2
50
.27
0.2
43
33
1¼
(ext
end>
37
ft)
270 MARINE MAMMAL SCIENCE, VOL. 19, NO. 2, 2003
Table1.
Con
tinued
.
Mea
nst
atis
tics
Tes
ts
Var
iab
len
ame
Des
crip
tion
Typ
eV
alu
esA
llse
tsW
ith
pin
ger
sW
ith
out
pin
ger
sE
nta
ng
leP
ing
sG
LM
exte
nd
dis
tan
ceb
etw
een
cork
lin
ean
dsu
rfac
efl
oats
(ft)
cnt
[12
,7
8]
38
.23
7.3
38
.23
3
mes
hst
retc
hed
mes
hsi
ze(i
n.)
cnt
[15
,2
2]
20
.32
0.4
20
.33
3m
esh
lo/h
i0¼
(mes
h<
20
)or
df0
,1g
0.5
10
.51
0.5
03
33
1¼
(mes
h.
20
)n
tcol
orco
lor
ofn
etca
tfg
reen
,re
d,
blu
e,b
row
n,
oth
erg
22
2,
24
,4
,6
4,
30
10
9,
13
,2
,3
1,
11
11
3,
11
,2
,3
3,
19
3
net
dp
thn
um
ber
ofm
esh
es,
cork
lin
eto
lead
lin
ecn
t[3
6,
1,0
50
]1
28
.51
28
.21
28
.83
3
net
len
len
gth
ofn
et(f
ath
oms)
cnt
[22
2,
1,0
00
]9
50
.79
49
.39
51
.73
3sl
ack
per
cen
tsl
ack
:ca
lcu
late
dfr
omn
um
ber
mes
hes
han
gin
gan
dh
ang
ing
len
gth
cnt
[0,
50
]4
2.1
42
.24
23
3
Location/seasonvariables
reg
ion
0¼
sou
thof
34
.58N
,ca
tf0
,1g
0.4
50
.46
0.4
43
33
1¼
nor
thof
34
.58N
lat
lati
tud
eat
star
tof
set
cnt
[30
,4
7]
34
.79
34
.87
34
.71
3lo
ng
lon
git
ud
eat
star
tof
set
cnt
[11
7,
12
6]
12
0.6
12
0.9
12
0.4
3
271BARLOW AND CAMERON: PINGERS REDUCE BYCATCH
Table1.
Con
tinued
.
Mea
nst
atis
tics
Tes
ts
Var
iab
len
ame
Des
crip
tion
Typ
eV
alu
esA
llse
tsW
ith
pin
ger
sW
ith
out
pin
ger
sE
nta
ng
leP
ing
sG
LM
area
Fiv
efi
shin
gre
gio
ns.
Reg
ion
s1
,3
,4
,5
sep
arat
edb
yla
titu
des
33
.838,
34
.338,
and
42
.008N
.R
egio
n2
com
pos
edof
smal
ldis
join
tar
eas
surr
oundin
gC
han
nel
Isla
nd
s.
cat
f1,...
,5g
31
5,
13
,7
,2
53
,2
1
16
1,
10
,5
,1
28
,1
0
15
4,
3,
2,
12
5,
11
mon
thm
onth
ofse
tca
tf1
,...
,1
2g
69
,0
,0
,0
,0
,0
,0
,5
4,
13
3,
15
7,
10
3,
93
36
,0
,0
,0
,0
,0
,0
,2
6,
66
,9
0,
48
,4
8
33
,0
,0
,0
,0
,0
,0
,2
8,
67
,6
7,
55
,4
5
3
272 MARINE MAMMAL SCIENCE, VOL. 19, NO. 2, 2003
Table2.
Fre
qu
ency
dis
trib
uti
onof
net
enta
ng
lem
ents
by
spec
ies
for
all
sets
,fo
rse
tsw
ith
pin
ger
s,an
dfo
rse
tsw
ith
out
pin
ger
s.
Sets
wit
hp
ing
ers
(n¼
29
5)
Sets
wit
hou
tp
ing
ers
(n¼
31
4)
All
#of
Enta
ngle
men
tsper
set
#of
Enta
ngle
men
tsper
set
Spec
ies
sets
12
3T
otal
12
3T
otal
Com
mon
dol
phin
,sh
ort-
bea
ked
24
33
17
22
1Delphinus
delphis
Com
mon
dol
phin
,lo
ng-b
eaked
10
11
Delphinus
capensis
Nor
ther
nri
gh
tw
hal
ed
olp
hin
81
35
5Lissodelphisborealis
Pac
ific
whit
e-si
ded
dol
phin
41
11
13
Lagenorhynchusobliquidens
Ris
so’s
dol
ph
in1
11
0Grampusgriseus
Dal
l’sp
orp
oise
31
12
2Phocoenoidesdalli
Shor
t-finned
pil
otw
hal
e1
01
1Globicephalamacrorhynchus
Sper
mw
hal
e1
11
0Physetermacrocephalus
‘‘Oth
erce
tace
ans’
’1
94
01
71
01
01
2(e
xclu
din
gsh
ort-
bea
ked
com
mon
dol
ph
in)
All
ceta
cean
s4
37
01
10
27
30
33
Nor
ther
nel
eph
ant
seal
13
33
10
10
Miroungaangustirostris
Cal
ifor
nia
sea
lion
18
44
14
14
Zalophuscalifornianus
All
pin
nip
eds
31
70
07
24
00
24
273BARLOW AND CAMERON: PINGERS REDUCE BYCATCH
program. Observers opportunistically recorded data on marine mammal sightingsduring the day as the vessel traveled from one location to another.
Data Selection
Experimental protocols were not followed on every set. Sometimes skippers chosenot to employ pingers in rough seas (18 cases), during the first set of a season or thefirst set with an inexperienced crew (7 cases), when pingers were causing problems (2cases), or for other reasons (20 cases). Occasionally, skippers chose to employ pingerseven when the protocol called for none (because marine mammals were known to bepresent, 5 cases). For analyses presented here, we excluded every set which did notfollow the experimental protocols. To prevent experimental manipulation of results,we also excluded all the sets from trips that were judged to be substantially out ofcompliance with experimental protocols (more than one-third of sets not followingprotocols). Of the 713 sets that were observed during the experiment, 104 wereexcluded, resulting in 609 sets that we included in our analyses.
Statistical Analyses
Descriptions and summary statistics for variables that are likely to affect marinemammal entanglement are given in Table 1. We use abbreviated variable names(Table 1) throughout this report. Some continuous variables and categoricalvariables with multiple states were collapsed to two-state categorical variables forsome analyses; for example, the number of chemical light sticks (‘‘sticks’’) wasincluded as a continuous variable and as the categorical variable ‘‘sticks present.’’
The random distribution of net and set variables in pingered and unpingeredsets was tested using the two-sample Wilcoxon rank sum test (two-tailed). Thereduction in marine mammal bycatch when pingers were present was tested usinga one-tailed Fisher’s exact test using a 2 3 2 contingency table (no entanglementsvs. one or more entanglements per set). Reduction in the number of entanglementsper set was tested with a non-parametric Wilcoxon rank sum test (one-tailed test).The distributions of fish catch were far from Poisson or normal; therefore, thereduction in the number of target and non-target fish caught was tested only withthe Wilcoxon rank sum test (one-tailed).
Multivariate tests of the effect of pingers and other variables on marine mammalentanglement were conducted using a Generalized Linear Modelling (GLM)framework (McCullagh and Nelder 1989). A logarithmic link function was used toapproximate a Poisson error structure:
lnðE½Yi�Þ ¼ b0 þX
Xijbj
where Yi is the number of entanglements for observation i, (for a species or speciesgroup); Xij is the value of predictor variable j for observation i, which may includemain effects and interaction terms; bj is the model coefficient for predictor variablej; and b0 is the coefficient for a constant term. The error structure was actuallyallowed to vary as
varðYiÞ ¼ r2 E½Yi�where the dispersion parameter, r2, can be estimated from the residuals toaccommodate deviations from Poisson expectations (r2 ¼ 1.0). Maximum
274 MARINE MAMMAL SCIENCE, VOL. 19, NO. 2, 2003
likelihood estimates of the coefficients, bj, were computed using iterativelyreweighted least squares using SPLUS software. According to likelihood theory,these parameters are asymptotically normal for known variance, hence, a t-test wasused to determine whether an estimated coefficient is significantly different fromzero.
Three pinger response variables (entanglements of ‘‘short-beaked commondolphin,’’ ‘‘other cetaceans,’’ and ‘‘pinnipeds’’) were modeled as linear functions ofpredictor variables including the number of pingers (‘‘pings’’), the number ofpingers squared (‘‘pings squared’’), and each variable indicated under the ‘‘GLM’’column of Table 1. A ‘‘net volume’’ term, the product of soak time, net length,and net depth, was included by adding soak time, net length, and net depthsimultaneously in a single model. Preliminary multivariate models were built usingan approximate stepwise approach implemented in SPLUS. These models were thenpruned by sequentially removing the least significant variable until all remainingvariables were statistically significant using a test for a reduction in overall deviance(a ¼ 0.05). For Poisson-distributed entanglements, a chi-square test was used formodel selection, and for over-dispersed models, an F-test was used (McCullagh andNelder 1989).
RESULTS
Entanglements
A total of 74 marine mammals (43 cetaceans and 31 pinnipeds) was entangled inthe 609 sets during the experiment (Table 2). Short-beaked common dolphins werethe most common species and accounted for over half of the cetaceanentanglements. Pinniped entanglements included northern elephant seals (Mir-ounga angustirostris) and California sea lions (Zalophus californianus) in roughly equalnumbers. For both cetaceans and pinnipeds, entanglement rates in nets withpingers were approximately one-third the rates in nets without pingers (Table 3).
Most marine mammal entanglements consisted of single individuals; however,three northern right whale dolphins (Lissodelphis borealis) were found entangled ina single net (with 24 pingers). The empirical distributions of the number ofentanglements per set for ‘‘short-beaked common dolphins,’’ ‘‘other cetaceans,’’ and‘‘pinnipeds’’ did not differ significantly from the Poisson distribution (chi-squaregoodness of fit, a ¼ 0.05).
Possible Confounding Factors
There were no significant differences between pingered and unpingered nets forany of the variables tested except for the number of light sticks (‘‘sticks’’ and ‘‘stickspresent’’). Geographic distributions of sets showed no obvious differences betweenpingered and unpingered sets (Fig. 1). Only two variables other than the number ofpingers were related to entanglement rates. Entanglement of short-beaked commondolphins was significantly related to the number of common dolphins sightings onthat trip (‘‘cdsight,’’ Wilcoxon rank sum test, P ¼ 0.0008). Entanglement of ‘‘othercetaceans’’ was not significantly related to any other variables. Entanglement ofpinnipeds was significantly related to the cloud cover at the end of the set (‘‘ecld lo/hi,’’ Wilcoxon rank sum test, P ¼ 0.04). Using a Bonferroni correction for multiple
275BARLOW AND CAMERON: PINGERS REDUCE BYCATCH
Table3.
Byc
atch
rate
san
don
e-ta
iled
stat
isti
cal
test
sof
dec
reas
esin
enta
ng
lem
ents
inse
tsw
ith
pin
ger
sco
mp
ared
tose
tsw
ith
out
pin
ger
s.
Byc
atch
rate
s(t
otal
byc
atch
/tot
alse
ts)
Stat
isti
cal
test
resu
lts
(P-v
alu
e)
Spec
ies
Sets
wit
hp
ing
ers
Sets
wit
hou
tp
ing
ers
Wil
coxo
nra
nk
sum
test
Fis
her
’sex
act
test
Com
mon
dol
phin
,sh
ort-
bea
ked
0.0
10
0.0
67
0.0
01
0.0
01
Delphinus
delphis
Com
mon
dol
phin
,lo
ng-b
eaked
0.0
00
0.0
06
0.2
27
0.2
58
Delphinus
capensis
Nor
ther
nri
gh
tw
hal
ed
olp
hin
0.0
10
0.0
16
0.0
70
0.1
24
Lissodelphisborealis
Pac
ific
whit
e-si
ded
dol
phin
0.0
03
0.0
10
0.3
17
0.3
29
Lagenorhynchusobliquidens
Ris
so’s
dol
ph
in0
.00
30
.00
00
.78
90
.48
5Grampusgriseus
Dal
l’sp
orp
oise
0.0
03
0.0
06
0.3
18
0.3
30
Phocoenoidesdalli
Shor
t-finned
pil
otw
hal
e0.0
00
0.0
03
0.2
27
0.2
58
Globicephalamacrorhynchus
Sper
mw
hal
e0
.00
30
.00
00
.22
70
.48
5Physetermacrocephalus
‘‘Oth
erce
tace
ans’
’0
.02
40
.04
10
.08
70
.12
7(e
xclu
din
gsh
ort-
bea
ked
com
mon
dol
ph
in)
All
ceta
cean
s0
.03
40
.11
0,
0.0
01
,0
.00
1N
orth
ern
elep
han
tse
al0
.01
00
0.0
32
0.0
36
0.0
56
Miroungaangustirostris
Cal
ifor
nia
sea
lion
0.0
14
0.0
45
0.0
13
0.0
20
Zalophuscalifornianus
All
pin
nip
eds
0.0
22
0.0
76
0.0
03
0.0
03
276 MARINE MAMMAL SCIENCE, VOL. 19, NO. 2, 2003
testing (a ¼ 0.05/19 ¼ 0.002), only one variable (the number of common dolphinsightings) remained significantly related to entanglements.
Pinger Effects on Entanglements of Short-beaked Common Dolphins
The bycatch of short-beaked common dolphins was significantly lower in netswith pingers (P ¼ 0.001, for both the one-tailed Wilcoxon rank sum test and theFisher exact test, Table 3). The only other variable that appeared to be statisticallysignificant was the number of common dolphin sightings on a trip (P , 0.001).The only variable selected in the stepwise log-linear model was the number ofpingers squared (P ¼ 0.0001, Table 4, Fig. 2).
Pinger Effects on Entanglements of Other Cetaceans
The bycatch of ‘‘other cetaceans’’ (other than short-beaked common dolphins)was not significantly related to pinger use in univariate tests (P ¼ 0.08 and P ¼0.13 using the one-tailed Wilcoxon rank sum test and the Fisher exact test,respectively) (Table 3). However, when the number of pingers used was included ina GLM model (as number of pingers squared), the pinger effect was statisticallysignificant (P ¼ 0.03, Table 4, Fig. 3). The only other significant variable in theGLM model was the Beaufort sea state at the end of the set. Pingers were notsignificantly related to entanglement rates for any of the other species testedseparately, but sample sizes were low in all cases (only one to eight totalentanglements per species). Entanglement rates were lower in pingered nets for fiveout of the seven other cetacean species.
Pinger Effects on Entanglements of Pinnipeds
Pinniped bycatch was also significantly lower in pingered nets (P ¼ 0.003 or0.003, one-tailed Wilcoxon rank sum test or the Fisher exact test, respectively)(Table 3). For individual species tested alone, bycatch reduction was significant forCalifornia sea lions (P ¼ 0.01 or 0.02, respectively) and marginally significant fornorthern elephant seals (P ¼ 0.04 or 0.06, respectively). The number of pingers(‘‘pings’’) was one of four significant variables selected in the stepwise building ofa GLM model for pinniped entanglement (P ¼ 0.007, Table 4, Fig. 4). The othersignificant variables in the GLM model were water ‘‘depth,’’ ‘‘gener,’’ and ‘‘engine.’’In univariate tests the only significant variable in explaining pinnipedentanglement was cloud cover (‘‘ecldlohi’’). This variable is not correlated withpinger use and cannot be used to explain the effect of pingers on entanglement.
Pinger Effects on Catch
There were no significant differences in the catch rates for the three target fishspecies (broadbill swordfish, common thresher shark, and shortfin mako shark)(one-tailed Wilcoxon rank sum test, Table 5). The catch rates of the non-target fishspecies were also not significantly related to pinger use (Table 5).
DISCUSSION
Pingers significantly reduced total cetacean and pinniped entanglement in driftgill nets without significantly affecting swordfish or shark catch. Results also
277BARLOW AND CAMERON: PINGERS REDUCE BYCATCH
Table
4.A
nal
ysis
ofdev
iance
table
sfo
rlo
g-l
inea
rfits
tom
arin
em
amm
alen
tangle
men
ts.
Init
ial
mod
els
buil
tusi
ng
appro
xim
ate
step
wis
eap
pro
ach
imp
lem
ente
din
SPL
US,
then
non
-sig
nifi
can
tva
riab
les
del
eted
(seq
uen
tial
lyre
mov
ing
leas
tsi
gn
ifica
nt)
un
til
rem
ain
ing
term
sal
lst
atis
tica
lly
sig
nifi
can
t(a
¼0
.05
).P
-val
ue
issi
gn
ifica
nce
leve
lfr
omei
ther
chi-
squ
are
test
or(f
or‘‘o
ther
ceta
cean
s’’)
app
roxi
mat
eF
-tes
tfo
rch
ang
ein
dev
ian
ce.
Mod
elR
esid
ual
dev
ian
ceD
egre
esof
free
dom
Ch
ang
ein
dev
ian
ceP
Est
imat
edco
effici
ent
Stan
dar
der
ror
ofco
effi
cien
t
Com
mon
dol
phin
(shor
t-bea
ked
)en
tangle
men
tm
odel
(est
imat
eddis
per
sion
¼1
.01
)G
ran
dm
ean
16
0.7
76
08
22
.72
10
.21
71
Pin
gs2
14
2.7
46
07
21
5.0
30
.00
01
20
.00
16
0.0
00
6
‘‘Oth
erce
tace
ans’’
enta
ng
lem
ent
mod
el(e
stim
ated
dis
per
sion
¼1
.26
)G
ran
dm
ean
14
1.1
26
08
23
.65
40
.29
61
Pin
gs2
13
5.4
36
07
25
.69
40
.03
20
.00
09
0.0
00
51
ebea
ulo
hi
13
0.7
46
06
24
.69
00
.05
1.0
23
0.5
55
Pin
nip
eden
tangle
men
tm
odel
(est
imat
eddis
per
sion
¼1
.01
)G
ran
dm
ean
18
7.4
06
07
22
.83
00
.20
61
Dep
th1
82
.46
60
62
4.9
40
.03
20
.00
06
50
.00
026
1P
ing
s1
75
.15
60
52
7.3
10
.00
72
0.0
31
0.0
11
1G
ener
17
0.7
06
04
24
.45
0.0
31
.09
00
.69
41
En
gin
e1
65
.87
60
32
4.8
30
.03
26
.73
01
0.3
5
278 MARINE MAMMAL SCIENCE, VOL. 19, NO. 2, 2003
indicate a greater reduction with a greater number of pingers. These results aresimilar to results of previous experiments that showed a significant reduction inharbor porpoise bycatch when pingers were used on set gill nets (Kraus et al. 1997,Larsen2, Trippel 1999, Gearin et al. 2000). Our experiment is, however, the firstunequivocal demonstration that pingers are correlated with a significant reductionin the bycatch for a delphinid cetacean (short-beaked common dolphin) and fora pinniped (California sea lion). The significant reduction in total cetacean bycatchwas largely driven by the reduction in bycatch of short-beaked common dolphins.Bycatch reduction was not statistically significant for any other cetacean species(although, bycatch was lower for most). An impractically large sample would berequired to find a statistically significant result for rare species, even if theirresponse was the same as for common dolphins.
Because of the potential importance of these results in reducing marine mammalbycatch worldwide, it is important to investigate potential spurious causes of thesepatterns. One potential concern is the lack of a true double-blind control in ourexperimental protocol. We cannot tell whether the observed pinger effect wascaused by the sound produced by the pingers or by the presence of something novelhanging from the net. We believe that the visual enhancement caused by thepresence of the pingers at night is trivial and that the sounds they emit almostcertainly caused the reduction in bycatch; however, our design does not allow us todistinguish between these hypotheses. A more serious concern is the possible director inadvertent manipulation of the results by the observers or the fishermen. Theobservers had no direct role in the design or analysis of the experiment and wouldnot directly benefit by manipulating the results (other than the common human
Figure 2. Predicted bycatch per set of short-beaked common dolphins as function ofnumber of pingers based on GLM. Dotted lines show approximate 95% confidence intervals.
279BARLOW AND CAMERON: PINGERS REDUCE BYCATCH
desire for successful outcomes). Fishermen knew that their industry was undergrowing scrutiny and that, if bycatch were not reduced, they might face additionalregulations or even closure; therefore, fishermen had a strong incentive to show thatpingers worked. The ability for fishermen to manipulate results was limited becausethe fishermen had already chosen a location before a set was determined to be‘‘pingered’’ or ‘‘unpingered.’’ Sets were eliminated from analysis when this protocolwas not followed. Once a net is set in a given location, there is little that a fishermancan do to affect marine mammal bycatch. Of the variables that are under a captain’scontrol (‘‘dlight,’’ ‘‘engine,’’ ‘‘gener,’’ ‘‘sticks,’’ ‘‘soak,’’ and ‘‘sonar’’), only ‘‘sticks’’ wassignificantly correlated with pinger use, and none were significantly correlated withcetacean bycatch. The effect of pingers on bycatch was greater than the effects of anyother variables (except number of common dolphin sightings), and it would beimpossible to contrive such a strong pinger effect by subtle experimentalmanipulations. Additional analyses (including classification and regression trees,CART) were conducted to look for other variables that might explain patterns ofentanglements,12 and pingers also emerged as an important explanatory variable inthose studies.
Figure 3. Predicted bycatch per set of ‘‘other cetaceans’’ (other than short-beakedcommon dolphins) as function of number of pingers based on GLM. Dotted lines showapproximate 95% confidence intervals.
12 Cameron, G. 1999. Report on the effect of acoustic warning devices (pingers) on cetacean andpinniped bycatch in the California drift gillnet fishery. Administrative Report LJ-99-08C(unpublished). 71 pp. Available from the Southwest Fisheries Science Center, 8604 La Jolla ShoresDrive, La Jolla, CA 92037, U.S.A.
280 MARINE MAMMAL SCIENCE, VOL. 19, NO. 2, 2003
Table5.
Cat
ch(n
um
ber
offi
sh)
and
one-
tail
edst
atis
tica
lte
sts
for
dec
reas
esin
catc
hra
tes
for
sets
wit
han
dw
ith
out
pin
ger
s.
Tot
alca
tch
Sets
wit
hp
ing
ers
Sets
wit
hou
tp
ing
ers
Wil
coxo
nra
nk
sum
Spec
ies
(#of
fish
)C
atch
Cat
ch/s
etC
atch
Cat
ch/s
etP
-val
ue
Tar
get
Swor
dfi
sh,
bro
adb
ill
1,0
75
51
31
.74
56
21
.79
0.4
6Xiphias
gladius
Shar
k,
Com
mon
thre
sher
46
21
70
0.5
82
92
0.9
30
.24
Alopius
vulpinas
Shar
k,
mak
o8
15
41
81
.42
39
71
.26
0.5
3Isurus
oxyrinchus
Non
-tar
get
Mol
a,co
mm
on2
,16
21
,01
23
.43
1,1
50
3.6
60
.43
Molamola
Op
ah6
07
30
61
.04
30
10
.96
0.3
0Lam
prisguttatus
Shar
k,
big
eye
thre
sher
69
25
0.0
94
40
.14
0.3
2Alopius
supersiliosus
Shar
k,
blu
e2
,11
91
,06
63
.61
1,0
53
3.3
50
.71
Prionaceglauca
Tu
na,
alb
acor
e1
,11
76
96
2.3
64
21
1.3
40
.46
Thunnus
alalunga
Tu
na,
blu
efin
57
22
95
1.0
02
77
0.8
80
.37
Thunnus
thynnus
Tu
na,
skip
jack
58
02
74
0.9
33
06
0.9
70
.32
Katsuwonus
pelamis
281BARLOW AND CAMERON: PINGERS REDUCE BYCATCH
Additional work is needed to determine the optimal number and placement ofpingers on drift gill nets. Log-linear models indicate that mortality rate is stilldecreasing with number of pingers within the range of 30–40 pingers (Fig. 2–4);however, there were few data during this experiment within the range of 1–20pingers, so there is considerable uncertainty about the shape of this response curvein that region. The GLM model identified Beaufort sea state, engine noise, andgenerator noise as possible explanatory variables in some analyses. All threevariables are sources of noise that might mask the sounds produced by pingers;however, engine and generator noise could also act to alert animals to the presenceof the net. Water depth is another explanatory variable for pinnipeds; this might beexpected because California sea lions forage only in the shallower, inshore portion ofthe operational range of drift gill net vessels.
The reduction we see in pinniped entanglements is particularly surprising becauseothers have predicted that pinnipeds might be attracted to nets to feed on thecaptured fish (the ‘‘dinner bell’’ effect). However, in an experimental study of theresponse of captive California sea lions to pingers, Anderson (2000) showed that theyinitially responded with a start followed by avoidance (five of six sea lions left thewater). This response helps explain the reduction we noted in sea lion entanglements.
Although pingers appear to reduce bycatch for a large range of marine mammalspecies, we echo the concerns that have been expressed by many other authors thatanimals may habituate to pingers. Given the relatively small number of nets andthe huge area fished, habituation may be less of a concern for the California driftgill net fishery than for intensive, localized set gill net fisheries in the Gulf of Maineand in the North Sea. We believe that pingers are unlikely to reduce the bycatch ofall cetacean species or all pinniped species.
Figure 4. Predicted bycatch per set of pinnipeds as function of number of pingers basedon GLM. Dotted lines show approximate 95% confidence intervals.
282 MARINE MAMMAL SCIENCE, VOL. 19, NO. 2, 2003
ACKNOWLEDGMENTS
We thank Tim Price and the hard-working fishery observers for collecting these data. Wethank the California drift gill net fishermen who have become actively involved in theprocess of improving their fishery. We are grateful to Rand Rasmussen for editing andmaintaining a reliable data base and Peter Perkins, Fred Julian and Cleridy Lennert for freelysharing their statistical expertise. Jim Carretta helped prepare Figure 1. Finally we wouldlike to thank all others who planned, funded, and helped carry out the pinger experimentwithin the California drift gill net monitoring program.
LITERATURE CITED
ANDERSON, R. C. 2000. Responses of captive California sea lions (Zalophus californianus) tonovel stimuli and the effects of motivational state. Master’s thesis, University of SanDiego, San Diego, CA. 192 pp.
CULIK, B. M., S. KOSCHINSKI, N. TREGENZA AND G. M. ELLIS. 2001. Reactions of harborporpoises Phocoena phocoena and herring Clupea harengus to acoustic alarms. MarineEcology Progress Series 211:255–260.
DAWSON, S. M. 1994. The potential for reducing entanglement of dolphins and porpoiseswith acoustic modifications to gillnets. Reports of the International WhalingCommission (Special Isssue 15):573–578.
GEARIN, P. J., M. E. GOSHO, J. L. LAAKE, L. COOKE, R. DELONG AND K. M. HUGHES. 2000.Experimental testing of acoustic alarms (pingers) to reduce bycatch of harbourporpoise, Phocoena phocoena, in the state of Washington. Journal Cetacean Research andManagement 2:1–9.
HATAKEYAMA, Y., K. ISHII, T. AKAMATSU, H. SOEDA, T. SHIMAMURA AND T. KOJIMA. 1994. Areview of studies on attempts to reduce the entanglement of the Dall’s porpoise,Phocoenoides dalli, in the Japanese salmon gillnet fishery. Reports of the InternationalWhaling Commission (Special Isssue 15):549–563.
JEFFERSON, T. A., AND B. E. CURRY. 1996. Acoustic methods of reducing or eliminatingmarine mammal-fishery interactions: do they work? Ocean and Coastal Management31:41–70.
JULIAN, F., AND M. BEESON. 1998. Estimates of marine mammal, turtle, and seabirdmortality for two California gillnet fisheries: 1990–95. Fishery Bulletin, U.S. 96:271–284.
KASTELEIN, R. A., D. DE HAAN, C. STAAL, S. H. NIEUWSTRATEN AND W. C. VERBOOM. 1995.Entanglement of harbour porpoises (Phocoena phocoena) in fishing nets. Pages 91–156 inP. E. Nachtigall, J. Lien, W. W. L. Au and A. J. Read, eds. Harbour porpoises—laboratory studies to reduce bycatch. De Spil Publishers, Woerden, The Netherlands.
KASTELEIN, R. A., H. T. RIPPE, N. VAUGHAN, N. M. SCHOONEMAN, W. C. VERBOOM AND
D. DE HAAN. 2000. The effects of acoustic alarms on the behavior of harbor porpoises(Phocoena phocoena) in a floating pen. Marine Mammal Science 16:46–64.
KRAUS, S., A. J. READ, A. SOLOW, K. BALDWIN, T. SPRADLIN, E. ANDERSON AND
J. WILLIAMSON. 1997. Acoustic alarms reduce porpoise mortality. Nature 388:525.MCCULLAGH, P., AND J. A. NELDER. 1989. Generalized linear models. Chapman and Hall,
New York, NY.PERRIN, W. F., G. P. DONOVAN AND J. BARLOW, EDS. 1994. Gillnets and cetaceans.Reports of
the International Whaling Commission Special Issue 15.TRIPPEL, E. A., M. B. STRONG, J. M. TERHUNE AND J. D. CONWAY. 1999. Mitigation of
harbour porpoise (Phocoena phocoena) by-catch in the gillnet fishery in the lower Bayof Fundy. Canadian Journal of Fisheries and Aquatic Science 56:113–123.
Received: 13 February 2002Accepted: 1 August 2002
283BARLOW AND CAMERON: PINGERS REDUCE BYCATCH