Introduction

The European eel Anguilla anguilla population has seriously declined throughout its distribution range during recent decades [1]. A number of causes have been suggested, including changes in ocean currents, climate change, obstructions to migration, habitat loss, parasites, virus infections, contaminants and over-fishing [2–7], and several causes may act in concert. Due to the population decline, the European eel has been included in the International Union for the Conservation of Nature and Natural Resources (IUCN) Red List of threatened species as critically endangered (http://www.iucnredlist.org/apps/redlist/details/60344/0). A European Union (EU) regulation has established measures for the recovery of the European eel, and requires that 40% of the pristine silver eel biomass from each river basin can migrate to the sea [8]. The still unknown reasons for the population decline, and the requirements of the EU regulation, necessitate more information on factors affecting the behavior, habitat use and migrations of the European eel, for example, [9, 10].

Electronic tags can be used to obtain information on European eel habitat use and migrations in freshwater and at sea [11, 12]. Optimal tagging methods are required to meet the ethical standards for use of research animals and to ensure that tagged fish exhibit a representative behavior. There are numerous tagging effect studies in other fishes, but few on eels [13]. Unique morphological, physiological and behavioral features of eels necessitate explicit evaluation and adjustment of handling and tagging methods. In anguilliform fishes, the physical dimensions or volume of a tag may be more important than that of mass [14], due to the narrow body cavity and anguilliforme swimming undulations.

There are three main methods for attaching large, electronic tags to fish, which are: 1) external attachment, 2) surgical implantation in the body cavity, and 3) gastric insertion via the mouth [13, 15, 16]. External attachment may be less suited for European eels due to their habitat use, as they are known to bury and hide in mud, gravel, vegetation and among stones and other structures [17]. This hiding behavior may increase the chances of losing external tags in eels and eel-like fishes [18, 19]. However, external tagging methods have been developed for external attachment of pop-up satellite archival transmitters to record silver eel ocean migrations [19, 20]. The present study focusses on surgical implantation and gastric insertion of tags.

One particular challenge when tagging eels is that they are able to turn their heads and bite their own incisions and sutures [personal observations, [21]. During surgical implantation, it may, therefore, be an advantage to place the incision as close to the head as possible to reduce this behavior. However, this increases the risk of cutting and damaging the liver with the scalpel during surgery, which may cause heavy bleeding [personal observation]. Information on the position of the liver is, therefore, needed for optimal placement of the incision. A second challenge is that the length of the body cavity limits the length of transmitters that can be surgically implanted. This is particularly an issue when developing long and flexible tags, for example, the modified G5 data storage tags, Cefas Technology Limited (CTL), UK., which consist of an electronic unit and three floats mounted on a titanium wire, the present model being 14 cm long in total [22, 23]. Data on the length of the body cavity provides information on how long such tags can be for silver eel of different body lengths.

Gastric insertion of tags requires the tag to be inserted via the mouth down the pharynx and into the stomach. The stomach length, therefore, limits the possible tag length. Furthermore, information on the position of the stomach is needed when inserting the tag, because the tag has to be inserted far enough to be placed in the stomach, but without rupturing the stomach wall or causing other physical damage to the fish.

The aim of this study was to collect anatomical measurements of length of the body cavity, distance from snout to the end the liver, length of the stomach and distance from the snout to the start of the stomach in European silver eel to provide recommendations on tag sizes and positions of surgically- and gastrically-implanted tags.

Methods

European silver eel (migration stage V [24]) were captured in a Wolf trap [25] close to the sea in the River Imsa in southern Norway, during downstream migration in October 2008, 2009 and 2010. The following measurements were collected from dead fish: fish body length (L T), length of body cavity, distance from snout to the end of the liver, distance from snout to the start of the stomach (that is, distance from snout to where the gall bladder is attached to the stomach), and distance from snout to the end of the stomach (defined here as the distance from the snout to where the stomach was too small for a 11 mm diameter tag, which is the diameter of the commonly available archival or acoustic tags, including the G5 tag). L T and one or several of the other measurements were taken for each individual, but not all measurements were taken for all individuals as measurements were done in connection with other studies. The total sample size was 95 eels, but the sample size for three of the analyses is lower (34 to 58 eels, see the Results section). The measurements are presented as a function of L T. Different models were tried for the relationship between L T and the other measurements. The model that according to the r2-values best described each of the relationships is presented.

Findings

The distance from the snout to the end of the liver (L EL) varied between 81 mm and 207 mm for silver eel between 380 mm and 931 mm body length (L T) (Figure 1). The relationship between L EL and L T was best described by a linear regression model (L EL = 0.22L T + 5.41, r2 = 0.92, n = 34).

Figure 1
figure 1

Relationship between distance from the snout to the end of the liver ( L EL ) and total body length ( L T ). The line shows the linear regression model (n = 34).

Full size image

Length of the body cavity (L BC) varied between 115 mm and 252 mm for silver eel between a body length (L T) of 380 mm and 931 mm (Figure 2). The relationship between L BC and L T was best described by a linear regression model (L BC = 0.23L T + 33.14, r2 = 0.95, n = 34).

Figure 2
figure 2

Relationship between length of the body cavity ( L BC ) and total body length ( L T ). The line shows the linear regression model (n = 34).

Full size image

Stomach length (L S) varied between 47 mm and 185 mm for silver eel between 380 mm and 998 mm body length (L T) (Figure 3). The relationship between L S and L T was best described by an exponential regression model (L S = 21.32e0.0019L T, r2 = 0.62, n = 58).

Figure 3
figure 3

Relationship between stomach length ( L S ) and total body length ( L T ). The line shows the exponential regression model (n = 58).

Full size image

Distance from the snout to the start of the stomach (L SS) varied between 67 mm and 190 mm for silver eel between 380 mm and 998 mm L T (Figure 4). The relationship between L SS and L T was best described by a linear regression model (L SS = 0.18L T + 0.32, r2 = 0.86, n = 95).

Figure 4
figure 4

Relationship between distance from the snout to the start of the stomach ( L SS ) and total body length ( L T ). The line shows the linear regression model (n = 95).

Full size image

Discussion

The results of this study provide useful information on eel anatomy for surgical and gastric implantation of tags in European silver eel. The results showed that the distance from the snout to the end of the liver constituted approximately one-fourth to one-fifth of the total body length of the fish (L T), indicating that optimal placement of the incision is slightly further from the head than one-fourth of L T to avoid damaging the liver. Further, the results showed that there was space for a 100 mm long tag (11 mm diameter) to be surgically implanted in all measured eels (that is, ≥380 mm L T). However, a 150 mm long tag could only be surgically implanted in silver eel longer than L T 550 mm. The narrow body cavity of eels limits the diameter of the tags that can be used. A previous study demonstrated that only silver eels >67 cm L T had a body cavity large enough to accommodate a 13 mm tag [23].

Surgical implantation of tags into the body cavity seems to be a suitable tagging method for European eel. Tag expulsion of surgically implanted tags may occur, but seems not to be a major problem based on studies of European eel and American eel Anguilla rostrata [21, 23, 26, 27]. In American eel, critical swimming velocity was not affected by surgically implanted tags [27]. Slow healing of the incision, inflammations and muscle necrosis at the incision does, however, appear to be a challenge, and previous studies have recommended closing the incisions using cyanoacrylate adhesive and a biological bandage made from the eel’s own fin [21, 26]. The risk with this method is that the cyanoacrylate may be shed relatively fast and the incision be left open [28]. It has later been recommended to close surgical incisions in European eel with monofilament sutures [23].

Gastric insertion of tags may decrease feeding and growth in tagged fish because the tag may block feed intake, the stomach volume available for ingesting feed is reduced, and the fish may feel satiated due to the mass and volume of the tag in the stomach [16]. However, a European silver eel has ceased feeding at this life stage [29], and there is no risk of affecting the feed intake. This may, therefore, be a suitable tagging method for this life stage in European eel. The metamorphosis from yellow eel to silver eel is a gradual process involving morphological and physiological changes, including regression of the alimentary tract as they cease feeding [24, 29, 30]. The question was, therefore, how much the alimentary tract was regressed and whether gastric insertion of tags was possible in silver eel at this stage. The length of the stomachs varied between 47 mm and 185 mm, indicating that there was space for short gastric tags in the smallest silver eels, but that there was space for relatively long tags in larger eels. Hence, the stomach was still sufficiently large for gastric insertion of tags at this stage. The results showed that the distance from the snout to the start of the stomach constituted 15 to 23% of L T, and indicated how far the transmitter should be inserted during the tagging procedure.

We know no published studies of the effects of intragastric insertion of tags in European eel. In a tagging effect study in American silver eel Anguilla rostrata, it was found that intragastrically inserted tags did not significantly impair swimming capacity or growth of the fish [27]. However, regurgitation was an issue because 28% of eels regurgitated their tags. The authors speculated that silver eel with degenerated alimentary tracts are less likely to regurgitate tags than yellow eel with functioning alimentary tracts [27]. At the same time the authors were worried that a degenerated alimentary tract may be more susceptible to puncture during transmitter insertion. Still, they did not find evidence of damage to the gut wall [27]. Hence, intragastric insertion of tags may be a quick and suitable tagging method in European silver eel, but more knowledge is needed on regurgitation rates and how to keep these as low as possible, and on the susceptibility of damaging the gut wall during tagging.