ICES CM2006/C:17
Mass occurrence of snake pipefish: result of a change in climate?
Cindy J.G. van Damme & A.S. (Bram) Couperus
IMARES, P.O. Box 68, 1970 AB IJmuiden, the Netherlands
Abstract
In 2004 a sudden mass occurrence of snake pipefish Entelurus aequoreus appeared in the
North-eastern Atlantic and has been increasing since. Before 2004 snake pipefish was mainly
found in coastal areas and occasionally in oceanic waters.
Indices (numbers of fish caught per hour) from inshore surveys remain at the same level,
while the indices from surveys conducted in deeper offshore areas show a very strong
increase since 2004. The length distributions of all surveys differ significantly from each
other. Coastal snake pipefishes are larger compared to pelagic specimens. Although the
outward appearance of the coastal pipefishes seems different from the pelagic specimens,
no differences were found when comparing taxonomic features. The mean numbers of rings
and fin rays are well within the ranges mentioned for snake pipefish. Apart from appearance
the habitat is different for the two types of snake pipefish. The oceanic form lives free in the
water column while the coastal form is found among sea weeds or in sea grass beds.
Although food is available in high quantities, the oceanic specimens of snake pipefish are
much leaner than the coastal specimens. While the snout length would make the species
more suitable for preying on less mobile prey, the stomach contents of the oceanic snake
pipefishes revealed remains of relatively small calanoids (mean length 2.4 mm). The calanoid
population has recently changed and is nowadays dominated by the smaller Calanus
helgolandicus. Here we put forward the hypothesis that the sudden appearance of the snake
pipefish in the deeper waters is a result of the change in the average lengths of calanoids
which in turn is caused by changes in the hydroclimatic environment.
The mass occurrence of the snake pipefish is affecting the whole ecosystem. Seabirds are
feeding their chicks with them and they are also found in stomachs of fish and sea mammals.
Keywords: snake pipefish, Entelurus aequoreus, climatic change, distribution, Atlantic
Contact author:
Cindy van Damme: IMARES, P.O. Box 68, 1970 AB IJmuiden, the Netherlands [tel: +31 255
564716, fax: +31 255 564644, e-mail: [email protected]].
Introduction
Pipefish (Syngnathidae) are marine fish that mostly inhabit inshore waters (Dawson 1986).
The snake pipefish (Entelurus aequoreus) is a species that can be found both in- and offshore
and in oceanic waters, though a review of the literature shows that there is some doubt
whether it is an in- or offshore species. At the end of the nineteenth and beginning of the
twentieth century snake pipefish is mostly described as an offshore fish found in deep
Atlantic waters (Couch 1877; Holt and Byrne 1904; Holt and Byrne 1906). Couch (1877)
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ICES CM2006/C:17
even gives ‘ocean pipefish’ as a synonym for Entelurus aequoreus. Some authors state that
there are two types of Entelurus; the larger oceanic and the smaller coastal form (Fries et al.
1895; Duncker 1915).Others even describe them as two separate species; E. aequoreus
that can be found in offshore and oceanic waters and E. anguineus which is found inshore
(Yarrel 1839; Moreau 1881). For some authors snake pipefish is an inshore fish (Day 1884;
Ehrenbaum 1909; Poll 1947).
In more recent fish guides snake pipefish is described as a species that can be found in
deeper coastal waters amongst large seaweeds (Wheeler 1969; Nijssen and De Groot 1980;
Dawson 1986; Muus et al. 1999) and most refer to the above references for the oceanic
occurrence. This is because in the second half of the last century only captures of snake
pipefish in coastal waters have been reported (Minchin and Molloy 1976; Briggs and McCurdy
1978; Andrews and Wheeler 1985).
Since 2004 high numbers of oceanic snake pipefish have been reported from pelagic cruises
and these have been rising ever since. In this paper we put forward the hypothesis that the
sudden appearance and mass occurrence of the snake pipefish in deeper oceanic waters is a
result of the change in the calanoid population which in turn is caused by changes in the
hydroclimatic environment.
Methods
Data on snake pipefish from international pelagic and demersal Atlantic and North Sea
surveys, International Bottom Trawl Survey (IBTS), Sole Net Survey (SNS), Demersal Fish
Survey (DFS), Herring Acoustic Survey (HERAS; Dutch participation), Blue Whiting Survey
(BWHTS; Dutch participation: from 2004 onwards) and Atlanto-Scandian Herring Survey (ASH;
European participation: from 2004 onwards), are used for the calculation of numbers present
and length-frequency distributions. BWHTS and ASH are pelagic surveys carried out in the
deeper waters of the North-eastern Atlantic in winter and spring, while HERAS is a pelagic
survey carried out in the deeper waters of the North Sea in summer. IBTS is a demersal
North Sea survey from which we only used the data from quarter 1, while SNS and DFS are
bottom trawl autumn surveys in the North Sea coastal zone.
Since 2004 snake pipefish have been collected for analyses during these surveys. Snake
pipefish, were counted and total length of each individual fish and total weight of all snake
pipefish were measured. Pipefish were either frozen for later analyses in the laboratory or
stored in 4% formaldehyde solution for stomach content analyses. Parameters measured in
the laboratory were total length, total weight, head length, snout length (from tip of the snout
to the vent), sex, trunk rings, tail rings, subdorsal rings (as described by Dawson (1986)),
dorsal fin rays and whether a brood pouch was present or not. The gastro intestinal tract was
dissected from the fish and cut open length ways. Since it was difficult to determine fullness
of the stomach, it was recorded as filled or empty. When possible remains were identified to
family level and length measured.
Results
The pelagic surveys are hydro acoustic single species surveys, targeting herring and blue
whiting. As a consequence catch data of other species are not readily available. However in
cruise reports from these surveys (unpublished data IMARES) it is reported that in 2004
snake pipefish suddenly appeared in the catches and in later years numbers increased.
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ICES CM2006/C:17
Figure 1 shows the presence of snake pipefish in the three demersal surveys. In 1983, 1989
and 1999 low numbers of snake pipefish were recorded during the IBTS survey. Also in 2002
and 2003 snake pipefish were occasionally caught. Since 2004 numbers have been
increasing, from 0.005 in 2003 to 5.1 pipefish per hour in 2006. In the coastal SNS and DFS
surveys snake pipefish have always been present in small numbers (Fig. 1), and no increase
is seen in the last three years.
Figure 2 a-d show the length distributions of the different surveys. Length distributions of all
surveys differ significantly from each other (P<0.0001). Comparison within the coastal
surveys or demersal or pelagic survey shows also a significant difference in length
distribution (P<0.0001). Mean lengths of the snake pipefish in the Atlantic BWHTS and ASH
are smallest (Table 1). While snake pipefish caught in the coastal zone (SNS/DFS) are larger
than those caught in the deeper North Sea (IBTS/HERAS).
Numbers in the DFS and SNS survey are very low. For BWHTS and ASH surveys it was
possible to compare length distributions of the last years. There is a significant (P< 0.0001)
difference between the years, with the largest fish caught in 2006 (Table 2).
Length distributions of BWHTS and ASH are clearly bimodal (Fig. 2c-d). The distribution of
IBTS is also slightly bimodal but not as clear as in the two other surveys. During the HERAS
survey snake pipefish were separated based on sex. Female snake pipefish are significantly
(P<0.001) larger than males (Fig. 3a-b & Table 3). The bimodality in the BWHTS, ASH and
IBTS is probably also due to differences in sex, rather than to different year classes.
The appearance of the coastal and oceanic specimens of snake pipefish is different (Fig. 4).
The oceanic form is much leaner and less brightly coloured compared tot the coastal form.
The snake pipefish caught in the ocean are lean, almost only scales and bones, and look like
they are starving. The coastal specimens are really fat, in that there is no lose skin and the
coloration is really bright. The specimens caught in the deeper North Sea are intermediate
between the oceanic and coastal appearance. They are not as lean as the oceanic ones, but
do show loose skin and colouration is brighter than but not as bright as the coastal form.
However when counting the rings on the body and dorsal fin rays of the pipefish no difference
is found between the oceanic, intermediate and coastal specimens. And the mean numbers
of rings and fin rays are well within the ranges mentioned for snake pipefish (Table 4). Also no
differences are found in the ring and fin ray counts between both sexes. In both the coastal
and pelagic specimens mature fish were found and males had brood pouches filled with
eggs, suggesting this is one species Entelurus aequoreus with different appearance in
different environments.
The diet of snake pipefish proved difficult to assess. A few had empty stomachs. Most of the
stomach contents were too far digested and impossible to identify (Table 5). What could be
identified were remains of calanoid copepods, though it was not possible to identify these to
species level. The mean length of these copepods was 2.4 mm (Table 5). The snout length
as proportion of the head length of the snake pipefish is 0.45 (Table 4). This proportion is
small compared to other pipefish species (Kendrick and Hyndes 2005), suggesting that the
snake pipefish head and snout is best suited for catching less mobile prey, such as
harpacticoid copepods and amphipods (Kendrick and Hyndes 2005).
Discussion
Historically snake pipefish was considered as a pelagic rather than as a coastal species. At
the end of the nineteenth and beginning of the twentieth century snake pipefish was almost
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ICES CM2006/C:17
only caught pelagic in deeper oceanic waters. This changed halfway the twentieth century
when catches were only reported from coastal areas. Since 2004 increasing numbers of
snake pipefish are suddenly appearing in oceanic waters and later on also in the deeper
waters of the North Sea. Kloppmann and Ulleweit (in press) also mention large catches of
snake pipefish in pelagic waters during plankton surveys in 2004. It looks like recently some
environmental change has lead to a mass occurrence of the snake pipefish in deep oceanic
waters comparable to the situation found at the beginning of the twentieth century.
Contrary to the coastal specimens that were always around in the coastal sea weed or sea
grass beds these oceanic snake pipefish live free high up in the water column and are not
associated with sea weeds. It has been suggested that the pelagic form might be the
juveniles of the coastal snake pipefish (Wheeler 1969). This could be true when looking at
mean length, the coastal specimens are larger compared to the pelagic specimens (Table 1).
However both in the pelagic and coastal appearance mature fish and males with full brood
pouches were found. Juveniles with mean length of 2.6 cm have been caught in the off shelf
areas in 2004 during a plankton survey (Kloppmann and Ulleweit in press). Juveniles have
also been reported from coastal sea grass beds (Vincent et al. 1995). This indicates that
both in- and offshore specimens are reproducing.
Although the pelagic specimens of snake pipefish are reproducing, they seem to be living in a
harsher environment than the coastal specimens. The pelagic specimens are found to be
leaner and less colourful compared to the coastal species. Duncker (1915) also mentions
that the pelagic form shows less pigmentation. Holt and Byrne (1906) describe the snake
pipefish as meagre and attenuate. It does not seem likely that a sudden shift has occurred
from coastal to offshore areas.
The proportion of the snout length of the head indicates that snake pipefish is adapted to
preying on less mobile prey (Table 4). In the Baltic, snake pipefish inhabiting coastal sea
grass areas have been found feeding on harpacticoid copepods (pers. comm. Anders
Svenson). However, since these copepods are living on sea weeds or the bottom, these are
not available in the water column of where the pelagic snake pipefish are found. The stomach
content analyses show remains of small calanoid copepods (Table 5). The two most
important calanoid copepod species in the North-eastern Atlantic in terms of biomass and
numbers are Calanus finmarchicus and C. helgolandicus (Williams et al. 1994; Gislason and
Astthorsson 1995). Recently there has been a major shift in the calanoid population caused
by changes in the climatic environment (Fromentin and Planque 1996; Planque and Fromentin
1996; Beare and McKenzie 1999). The smaller Calanus helgolandicus has become much
more important and is now dominating the copepod population in both the North-eastern
Atlantic and the North Sea (Fromentin and Planque 1996; Planque and Fromentin 1996;
Beare and McKenzie 1999). The mean total length of calanoid copepods found in the
stomachs of the pelagic snake pipefish is 2.4 mm (Table 5). This is within the size range of
Calanus helgolandicus. It seems that the pelagic snake pipefish might have profited from the
shift to the smaller calanoid copepod. And the mass occurrence might therefore be an
indirect effect of climatic change. Some care should be taken since the shift of the calanoid
population already started at the end of the twentieth century while the sudden mass
occurrence of the snake pipefish only started in 2004. However, a time lag between optimum
conditions causing increased breeding success and mass appearance is to be expected,
because of the limited number of eggs that are produced per specimen in pipefishes. Snake
pipefish like other pipefish develop their eggs in the male brood pouch and therefore
numbers of eggs produced per fish are lower compared to free egg spawning species.
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ICES CM2006/C:17
It might be that the mass occurrence of the pelagic snake pipefish is caused by a strong year
class, but it is not possible to prove this with the collected data. The fact that the mean total
length increases over the year could indicate that this is just one strong year class. However
the fact that the numbers of snake pipefish caught over the years are rapidly increasing,
despite the fact that this species produces relatively few eggs, seems to disapprove this
hypothesis.
Whether or not the mass occurrence is just one strong year class, it is affecting the
ecosystem. Seabirds are found preying on and feeding their chicks with the snake pipefish
(Harris 2006). Also fish caught in pelagic trawls were found with stomachs stuffed of the
pipefish. Even dolphins that are bycaught in pelagic trawls were found to have preyed on
snake pipefish. This has also been recorded at the end of the nineteenth century when snake
pipefish were also found in pelagic waters in high numbers. Couch (in Fries et al. 1895)
reported pollack that had their stomachs stuffed with snake pipefish.
It would be of scientific interest to keep investigating the development in the snake pipefish
population as well as in others species, such as for example in deal fish, Trachipterus
arcticus, another rare species in the pelagic ecosystem that showed up in large numbers in
pelagic surveys in 2006. Investigations of mass occurrences in these non commercial
species may help us to understand the causes and the implications of major changes in the
marine ecosystem that seem to happen in the course of time, more noticeably in the last
decade.
References
Andrews MJ, Wheeler A (1985) Rare and little-known fishes in the Thames Estuary. Journal of
Fish Biology 27: 59-71
Beare DJ, McKenzie E (1999) Temporal patterns in the surface abundance of Calanus
finmarchicus and C. Helgolandicus in the northern North Sea (1958-1996) inferred
from Continuous Plankton Recorder data. Marine Ecology Progress Series 190: 241251
Briggs RP, McCurdy WJ (1978) Marine fishes taken in waters off the North coast of Ireland
during 1977. Ir. Nat. J. 19: 267-268
Couch J (1877) A history of the fishes of the British Isles
Dawson CE (1986) Syngnathidae. In: Whitehead PJP, Bauchot M-L, Hureau J-C, Nielsen J,
Tortonese E (eds) Fishes of the North-eastern Atlantic and the Mediterranean.
UNESCO, Paris, pp 628-639
Day F (1884) The fishes of Great Britain and Ireland. Williams and Norgate, London
Duncker G (1915) Revision der Syngnathidae. Mitteilungen aus dem Naturhistorischen
museum in Hamburg 32: 32-34
Ehrenbaum E (1909) Eier und Larven von Fischen. Lipsius & Tischer, Kiel und Leipzig
Fries B, Ekström CU, Sundevall C (1895) A history of Scandinavian fishes. Norstedt & Söner,
Stockholm
Fromentin J, Planque B (1996) Calanus and environment in the eastern North Atlantic. II.
Influence of the North Atlantic Oscillation on C. finmarchicus and C. helgolandicus.
Marine Ecology Progress Series 134: 111-118
Gislason A, Astthorsson OS (1995) Seasonal cycle of zooplankton southwest of Iceland.
Journal of Plankton Research 17: 1959-1976
Harris M (2006) Seabirds and pipefish: a request for records. British birds 99: 148
5
ICES CM2006/C:17
Holt EWL, Byrne LW (1904) On the fishes taken by the Oceana. Annals of natural history or
Magazine of Biology, Botany and Geology 14: 37-40
Holt EWL, Byrne LW (1906) First report on the fishes of the Irish Atlantic slope. Fisheries
Ireland, Scientific Investigations II
Kendrick AJ, Hyndes GA (2005) Variations in the dietary compositions of morphologically
diverse syngnathid fishes. Environmental Biology of Fishes 72: 415-427
Kloppmann MHF, Ulleweit J (in press) Off-shelf distribution of pelagic snake pipefish, Entelurus
auquoreus (Linnaeus, 1758), west of the British Isles
Minchin D, Molloy J (1976) Notes on fishes taken in the Irish waters. Ir. Nat. J. 18: 360-363
Moreau E (1881) Histoire Naturelle des Poissons de la France. Libraire de l' academie de
Medecine, Paris
Muus BJ, Nielsen JG, Dahlstrom P, Nystrom BO (1999) Zeevissen van Noord- en WestEuropa. Schuyt & Co Uitgevers en Importeurs, Haarlem
Nijssen H, De Groot SJ (1980) Zeevissen van de Nederlandse kust. Wetenschappelijke
mededelingen KNNV 143: 109
Planque B, Fromentin J (1996) Calanus and environment in the eastern North Atlantic. I.
Spatial and temporal patterns of C. finmarchicus and C. helgolandicus. Marine
Ecology Progress Series 134: 101-109
Poll M (1947) Poissons Marins, Bruxelles
Vincent ACJ, Berglund A, Ahnesjö I (1995) Reproductive ecology of five pipefish speciesin one
eelgrass meadow. Environmental Biology of Fishes 44: 347-361
Wheeler A (1969) The fishes of the British Isles and North West Europe. Macmillan, London
Williams R, Conway DVP, Hunt HG (1994) The role of copepods in the planktonic ecosystems
of mixed and stratified waters of the European shelf seas. Hydrobiologia 293: 521530
Yarrel W (1839) Remarks on one species of the genus Syngnathus. Annals of natural history
history or Magazine of Biology, Botany and Geology 3: 81-85
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ICES CM2006/C:17
Figure 1. Mean number per hour of snake pipefish caught over the years during the IBTS,
SNS and DFS surveys.
0.16
6
0.14
5
0.1
0.08
3
0.06
2
0.04
1
0.02
7
2002
1997
1992
1987
1982
1977
0
1972
0
1967
N/hour IBTS
4
N/hour SNS-DFS
0.12
IBTS
SNS
DFS
ICES CM2006/C:17
Figure 2. Length frequency distribution of snake pipefish caught during the different surveys;
A = SNS/DFS (1969-2005), B = IBTS (2002-2006), C = BWHTS, D = ASH.
20
250
A
B
200
Number
Number
15
SNS
10
DFS
5
150
IBTS
100
50
0
0
1
6
11
16
21
26
31
36
41
46
51
1
6
11
16
21
Length (cm)
26
31
36
41
46
51
Length (cm)
30
80
C
D
25
60
2004
Number
Number
20
2005
15
2006
2004
40
2005
2006
10
20
5
0
0
1
6
11
16
21
26
31
36
41
46
51
1
Length (cm)
6
11
16
21
26
31
Lenght (cm)
8
36
41
46
51
ICES CM2006/C:17
Figure 3A. Length frequency distribution of the different sexes of snake pipefish caught
during the Herring acoustic survey (HERAS).
50
Number
40
30
female
male
20
10
0
1
6
11
16
21
26
31
Length (cm)
9
36
41
46
51
ICES CM2006/C:17
Figure 3B. Length- weight relationships of male and female snake pipefish.
18
16
y = 7E-05x 3.0629
R2 = 0.687
14
Weight (g)
12
female
10
male
8
y = 9E-06x 3.7861
R2 = 0.8776
6
4
2
0
0
10
20
30
40
Length (cm)
10
50
ICES CM2006/C:17
Figure 4. Coastal (A), intermediate (B, C) and pelagic (D) specimens of snake pipefish.
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ICES CM2006/C:17
Table 1. Mean lengths of snake pipefish in the different surveys
SNS
37.9
6.5
1.4
20
46
21
Mean
Std dev
Std err
Min
Max
N
DFS
38.4
5.0
0.9
14
53
79
IBTS
32.2
5.4
0.1
9
48
2052
HERAS
32.9
5.0
0.3
21
46
397
BWHTS
25.7
6.0
0.3
13
40
443
ASH
29.0
5.6
0.2
15
57
986
Table 2. Mean lengths of snake pipefish in the last three years of the BWHTS and ASH
surveys.
BWHTS
2005
23.1
5.6
0.4
13
40
214
2004
23.4
2.9
0.7
15
26
18
Mean
Std dev
Std err
Min
Max
N
ASH
2006
28.5
5.4
0.4
13
40
211
2005
27.4
5.4
0.4
15
40
161
2006
29.3
5.5
0.2
17
57
211
Table 3. Difference of mean lengths of the different sexes for snake pipefish caught during
the HERAS survey.
female
35.9
2.7
0.2
24
43
194
Mean
Std dev
Std err
Min
Max
N
male
27.5
3.1
0.3
22
35
86
Table 4. Biological parameters of snake pipefish.
Mean
Min
Max
N
♀
Length
(cm)
35.5
21.5
47.1
223
♀
Weight
(g)
3.4
1
16.1
29
♂
Length
(cm)
26.3
17.7
37.3
116
♂
Weight
(g)
1.2
0.4
7
29
Snout as
proportion
of head
length
0.45
0.31
0.53
66
12
Trunk
rings
29.5
27
36
61
Tail
rings
61.5
43
67
61
Subdorsal
rings
8.4 + 3.2
7+2
10 + 4
61
Dorsal
fin
rays
39.7
34
46
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ICES CM2006/C:17
Table 5. Unidentifiable matter in the stomachs of snake pipefish and sizes of Calanus found.
Mean
Min
Max
N
Mean %
unidentifiable
matter
92.5
70
100
10
Body length
(mm)
Tail length
(mm)
Total length
(mm)
2.1
1.7
2.7
9
0.5
0.5
0.5
3
2.4
2.2
2.5
3
13