Mass Occurrence of Snake Pipefish: Result of a Change in Climate? ICES

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)

1 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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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

3 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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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: 241- 251 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

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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 West- Europa. 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: 521- 530 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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Figure 1. Mean number per hour of snake pipefish caught over the years during the IBTS, SNS and DFS surveys.

6 0.16

0.14 5

0.12

4 0.1 IBTS 3 0.08 SNS DFS

N/hour IBTS N/hour 0.06 2 SNS-DFS N/hour 0.04

1 0.02

0 0 1967 1972 1977 1982 1987 1992 1997 2002

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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 15

150 SNS 10 IBTS DFS

Number Number 100

5 50

0 0 1 6 11 16 21 26 31 36 41 46 51 1 6 11 16 21 26 31 36 41 46 51 Length (cm) Length (cm)

30 80 C D 25 60 20 2004 2004 15 2005 40 2005 Number 2006 Number 2006 10 20 5

0 0 1 6 11 16 21 26 31 36 41 46 51 1 6 11 16 21 26 31 36 41 46 51 Length (cm) Lenght (cm)

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Figure 3A. Length frequency distribution of the different sexes of snake pipefish caught during the Herring acoustic survey (HERAS).

30 female male Number 20

0 1 6 11 16 21 26 31 36 41 46 51 Length (cm)

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Figure 3B. Length- weight relationships of male and female snake pipefish.

16 y = 7E-05x3.0629 14 R2 = 0.687 12 female 10 male 8 3.7861 Weight (g) y = 9E-06x 6 R2 = 0.8776 4

0 0 1020304050 Length (cm)

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Figure 4. Coastal (A), intermediate (B, C) and pelagic (D) specimens of snake pipefish.

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Table 1. Mean lengths of snake pipefish in the different surveys

SNS DFS IBTS HERAS BWHTS ASH Mean 37.9 38.4 32.2 32.9 25.7 29.0 Std dev 6.5 5.0 5.4 5.0 6.0 5.6 Std err 1.4 0.9 0.1 0.3 0.3 0.2 Min 20 14 9 21 13 15 Max 46 53 48 46 40 57 N 21 79 2052 397 443 986

Table 2. Mean lengths of snake pipefish in the last three years of the BWHTS and ASH surveys.

BWHTS ASH 2004 2005 2006 2005 2006 Mean 23.4 23.1 28.5 27.4 29.3 Std dev 2.9 5.6 5.4 5.4 5.5 Std err 0.7 0.4 0.4 0.4 0.2 Min 15 13 13 15 17 Max 26 40 40 40 57 N 18 214 211 161 211

Table 3. Difference of mean lengths of the different sexes for snake pipefish caught during the HERAS survey.

female male Mean 35.9 27.5 Std dev 2.7 3.1 Std err 0.2 0.3 Min 24 22 Max 43 35 N 194 86

Table 4. Biological parameters of snake pipefish.

Snout as ♀ ♀ ♂ ♂ proportion Dorsal Length Weight Length Weight of head Trunk Tail Subdorsal fin (cm) (g) (cm) (g) length rings rings rings rays Mean 35.5 3.4 26.3 1.2 0.45 29.5 61.5 8.4 + 3.2 39.7 Min 21.5 1 17.7 0.4 0.31 27 43 7 + 2 34 Max 47.1 16.1 37.3 7 0.53 36 67 10 + 4 46 N 223 29 116 29 66 61 61 61 58

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Table 5. Unidentifiable matter in the stomachs of snake pipefish and sizes of Calanus found.

Mean % Body length Tail length Total length unidentifiable (mm) (mm) (mm) matter Mean 92.5 2.1 0.5 2.4 Min 70 1.7 0.5 2.2 Max 100 2.7 0.5 2.5 N 10 9 3 3