The Entelurus aequoreus

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Introduction -

The Snake pipefish Entelurus aequoreus (Linnaeus, 1758), belongs to the Syngnathidae family which also includes seahorses. This family share a recognisable characteristic of a long broad snout from which the name Syngnathidae is derived. They live in temperate waters in the eastern Atlantic from the Azores to Iceland and Norway. Some can be found living pelagicaly in the open ocean whereas others are demersal living in shallow habitats associated with algae (Polte & Buschbaum, 2008; Kloppmann & Ulleweit, 2007). It appears that there are some very distinct differences in the appearance of oceanic and coastal snake pipefish. Coastal dwellers have a longer, more rotund body and brighter orange colouration, whereas oceanic pipefish are much thinner and have a duller colouration. Also individuals caught in the deeper North Sea areas seem to be an intermediate between the two (van Damme & Couperus, 2008). It has been suggested that the habitat preference changes with life stage or that there are two distant taxonomic groups (Polte & Buschbaum, 2008), however analysis by van Damme and Couperus (2008) suggest that they are the same species; counts of the rings on the body and dorsal fin rays revealing no significant difference between the two life strategies.

There are many conflicting opinions as to whether the snake pipefish was originally an oceanic or coastal species. It seems that in the early 1900s the pipefish's habitat was described as oceanic or pelagic and mostly caught in deeper waters (Holt & Byrne 1906). However this changed in 20th century when they appeared mostly in coastal areas. ( reference )

Entelurus feed on zoobenthos and zooplankton such as fish eggs and larvae and other planktonic crustaceans, that they suck up using there tube- like snouts (FishBase 2009)., Hhowever more detailed analysis of stomach contents of pipefish living in Japanese seaweed beds, has revealed a high abundance of harpacticoid copepods (Polte & Buschbaum, 2008).), then again however this data may be biased towards prey availability in this area and not an accurate assessment of widespread prey. Although, Tripton and Bell (1988) have described the harpacticoid copepod as an important food source for other species of pipefish, van Damme and Couperus (2008) looked at the stomach contents of a range of pipefish caught in the northeast North Sea, they could not identify the contents to species level due to the level of digestion. However they were identified as calanoid copepods with their mean length suggesting they may be Calanus helgolandicus.

The Syngnathidae family have an unusual reproductive strategy as it is the male that carries the fertilised eggs (Wilson et al. 2003), the females lay the eggs in the males brood pouch on the abdomen (Kirby et al. 2006). The eggs will remain within this pouch for between one and two months, however the breeding season usually extends between May and late August , so that the males can often incubate more than one brood in a season depending on the environmental conditions (Ahnesjo, 2008). Brooding also reportedly occurs at different times in the coastal and oceanic types, water is colder in oceanic areas but pipefish are found to breed/spawn in march and April, possibly enabling juveniles to take advantage of the low metabolic costs at these temperatures, as food supply is scarce, therefore aiding juvenile survival at this critical stage (Kloppmann & Ulleweit, 2007). In contrast coastal juveniles are usually found between June and July as this is when waters are warmer and prey availability is high (Dawson 1986).

Currently there are a number of papers documenting an increase of snake pipefish in the North Sea and surrounding areas since the early 2000s both in trawl and Continuous Plankton Recorder (CPR) surveys. However sightings by divers and fishermen have also increased to a great extent (Harris et al. 2006).

The increased was first published around 2006; Lindley et al. (2006) reported an exceptional increase in pipefish in continuous plankton recorder (CPR) surveys starting in 2003 in the waters west of the Irish coast. Larval and juveniles where caught and then genetically analysed to determine that they were E. aequoreus. Also at this time E. aequoreus began to appear in standard trawl surveys (Harris et al 2007). Standard trawl surveys are undertaken within the parameters set out by the international bottom trawl survey working group, results are standardised as pipefish caught h-1, this data is amalgamated by the Fisheries research servies services (FRS) trawl survey data base. A standard survey follows the same operating procedures as the ICES trawl surveys (as described in the materials and methods section).

The increase became an issue in the ecological sense when it was reported that E. aequoreus had started to become part of the diet of sea birds and other marine predators (Harris et al 2008). This is an issue for sea birds as they are already under stress as their main food source, the Lesser sandeel Ammodytes marinus, have been the victim of continual overfishing recently (Mavor et al 2005, 2006). Pipefish are a poor alternative prey as they have very little nutritional value compared to the sandeel, also their tough rigid bodies make them very difficult to swallow and digest. Many deaths from starvation and chocking have been recorded in both adults and chicks. Analysis shows that pipefish contain a very small amount of lipid and large amount of ash. Average ash content as a percentage of dry weight 24.69± 0.77 in Snake pipefish compared to 12.54± 0.28 % in 0-group sandeel (Method and results, Harris et al 2008). Previous work has shown that most colonies have less successful breeding years when feeding chicks on lower than average lipid and energy content (Wanless et al., 2005). In addition Speakman (1987) has hypothesised notised that a high amount of ash may affect absorption of other food ingested simultaneously.

Other marine species found to be feeding on pipefish include mackerel Scomber scombrus, shortbeaked common dolphins Delphinus delphis (van Damme and Couperus, 2008)and , bass Dicentrarchus labrax (Lancaster, pers. comm.).

There have been suggestions as to the cause of this increase, the main one being an increase in sea surface temperature (SST) in the northern hemisphere (Kirby et al. 2006). Not only would a rise in northern hemisphere temperature increase the ecological niche of the pipefish, therefore enabling populations and individuals to move into sea areas where they where not previously found, but also a rise of a few degrees in water temperature has a physiological effect on the pipefish. Ahnesjö (1995) found that in another species, Sygnathus typhle, an increase in temperature from 10 -15°c will on average reduce incubation time of the eggs in the males brood pouch by 23 days. The males can therefore brood more offspring throughout one season. This physiological effect of increased water temperature is also thought to occur in E. aequoreus.

Another suggested reason for the increase in the E. aequoreus population has been put forward by Polte and Christian (2008). They state that pipefish have a new habitat thanks to the introduced seaweed Sargassum muticum. Not only does this newly introduced Japanese seaweed provide perfect cover for pipefish during the breeding season, it has also been shown that there are higher concentrations of zooplankton within the bed, especially harpacticoid copepods, their favoured prey. The distribution of food source could also play a part, as there has found to be a shift in the usual planktonic structure, in this area. Calanoid copepods have been found to be shifting northwards in distribution, whereas there has been an overall decrease in Calanus populations in UK waters (Johns and Haliday, 2007). At present there are many changes in the marine ecosystem occurring and many papers show this to be an effect of fishing (eg. Daan et al., 2005; Jennings et al., 1999, 2001, 2002) and ecosystem change first starts to become visible in the planktonic populations. Shifts have also occurred due to climatic changes, and therefore favouring the smaller species C. helgolandicus (van Damme and Couperus, 2008). Changes in climatic are associated with warming of the oceans, these warmer temperatures favour smaller species as water become more stratified therefore preventing upwelling of nutrients. As a result larger celled phytoplankton cannot sustain themselves in this nutrient limited environment and consequently retreat to colder areas. Smaller species are then able to dominate as there metabolic needs are less (Richardson & Schoeman, 2004, Beaugrand &Reid, 2003).

It is not known whether this change in snake pipefish abundance is just a sudden increase in overall abundance or a gradual movement of the entire population in to the North Sea and surrounding areas. In order to investigate this trawl surveys from other areas surrounding the north sea and each zone of the north sea individually will be looked at.

The aim of this project is to build on current literature reports of the increase in abundance and distribution of snake pipefish in the North Sea, however little is known about what is actually happening to initiate such a dramatic response. (There have some hypotheses suggesting possible expiations for this phenomenon, all mainly link in with the topical subject of climate change including increasing sea surface temperatures in this area, which has also resulted in the movement of one of their main food sources, Copepods (Beaugrand et al.,2002), I will also aim to determine whether E. aequoreus have gradually moved in to the north sea from other areas or indeed whether all areas experienced a population explosion during the same time frame . In order to achieve this data of E. aequoreus abundance from trawl surveys taken in the North Sea will be used and also try to demonstrate the link between climate change and changes in abundance, by looking at temperature data in relation to the abundance data.

The data used in this project was not collected by myself but comes from the following sources :

Raw data used in this project for analysing pipefish abundance in the North Sea is supplied by the ICES online database survey ( ICES (The International Council for the Exploration of the Sea) work alongside research scientists and many countries in order to coordinate research of the marine environment. The online data base contains data from the area shown in figure 1. This areas is then divided into sub areas and then again in to smaller ICES rectangles. This makes it easier when organising surveys. I used data from the IBTS-NS (International bottom trawl survey - North sea).The North sea is dived in to three sub area IVa, IVb and IVc and data from all three of these area have been incorporated in order to identify total abundance in the north sea. I will also look at each sub area separately, in order to see whether there has been any gradual movement into the North Sea. The IBTS survey has been running since the 1960s, however was only standardised in the early 80's. Since this point all ships use the GOV (Grande Overture Verticale) trawl, trawling at the speed of 4 knots for 30 minuets (ICES, 2010). The catch is then expressed as number per hour. ICES surveys are conducted in the first and third quarters of each year. The survey also records length, sex and day/night but this was not relevant for my project, so these data were discarded.

There are 8 countries involved in carrying out trawls in the IBTS survey; each country is responsible for surveying a particular area, and this takes place within a specified time. The GOV trawl used was specifically designed by the French Research Institute for Exploitation of the Sea(IFREMER) for use in these research projects. A 30mm mesh is used to line the cod end so that smaller, younger fish will remain in the net, in order that they can be examined and included in the record. (Fisheries Research Services, 2010)

This data will be analysed along with sea surface temperature data and copepod abundances in the North Sea to prove any links between this and pipefish abundance.

The northern hemisphere temperature data used is from the University of East Anglia, climate research unit.It shows temperature anomalies deviating away from the long term average in the northern hemisphere. The sea surface temperate data is collected voluntarily by merchant and navy vessels, however the problem with this method of collection is that data samples collected are in essence restricted to main shipping roots and they may not give an accurate overview of the whole area ( maps of the areas covered can be found in Rayner et al. (2003)) . The long term average was calculated using all the temperature data from 1961 -1990.

In order to get an idea of distribution of the E . aequoreus the north sea data is separated into it s three ICES zones I V a, IVb and IVc . An average is then taken for each of these zones on a year to year basis , because they are not all the same size and therefore an average will give a more accurate repre se ntation of total abundance a nd also to indicate when the increase s are occurring in each zone.

An ANCOVA test will be used on the abundance data to confirm any significant changes in abundance.