From yellow to silver: Transforming cranial morphology in European eel (Anguilla anguilla).

The European eel (Anguilla anguilla) has been extensively studied, especially because of its highly specialized migratory behaviour associated with substantial phenotypic transformations. During this migration, one of those transformations the eel undergoes is from yellow to silver eel, a process known as silvering. Although the cranial morphology during the earlier glass, elver and yellow eel stages are well studied, little is known about actual morphological changes during the transformation process from the yellow to the silver eel stage. Yet, literature suggests drastic changes in musculoskeletal anatomy. Here, we investigated the cranial musculoskeletal morphology of 11 male European eels at different stages during silvering, resulting both from natural and artificial maturation. Using 3D-reconstructed µCT data of the head, the skull and cranial muscles associated with jaw closing and respiration were studied. Eye size was used as a proxy for the silvering stage. Size-adjusted jaw muscle volumes increased during silvering, although insignificantly. Accordingly, a near-significant increase in bite force was observed. Respiratory muscles size did increase significantly during silvering, however. Considering the eel's long migration, which often includes deep and thus potentially oxygen-poor environments, having a better performing respiratory system may facilitate efficient migration. Both overall skull dimensions and specifically orbit size increased with eye index, suggesting they play a role in accommodating the enlarging eyes during silvering. Finally, artificially matured eels had a wider and taller skull, as well as larger jaw muscles than wild silver eels. This could be caused (a) by different conditions experienced during the yellow eel stage, which are maintained in the silver eel stage, (b) by side effects of hormonal injections or (c) be part of the maturation process as artificially induced silver eels had a higher eye index than the wild silver eels.

Burrowing behaviour of the European eel (Anguilla anguilla): Effects of life stage.

The European eel (Anguilla anguilla) is a fascinating species, exhibiting a complex life cycle. The species is, however, listed as critically endangered on the IUCN Red List due to an amalgam of factors, including habitat loss. This study investigated the burrowing behaviour and substrate preference of glass, elver and yellow stages of A. anguilla. Preference was determined by introducing eels in aquaria with different substrates and evaluating the chosen substrate for burrowing. In addition, burrowing was recorded using a camera in all substrate types and analysed for kinematics. The experiments showed that all of these life stages sought refuge in the sediments with particle sizes ranging from sand to coarse gravel. Starting from a resting position, they shook their head horizontally in combination with rapid body undulations until half of their body was within the substrate. High-speed X-ray videography revealed that once partly in the sediment, eels used only horizontal head sweeps to penetrate further, without the use of their tail. Of the substrates tested, burrowing performance was highest in fine gravel (diameter 1-2 mm; lower burrowing duration, less body movements and/or lower frequency of movements), and all eels readily selected this substrate for burrowing. However, glass eels and elvers were able to use coarse gravel (diameter >8 mm) because their smaller size allowed manoeuvring through the spaces between the grains. Further, burrowing performance increased with body size: glass eels required more body undulations compared to yellow eels. Interestingly, the urge to hide within the sediment was highest for glass eels and elvers. Documentation of substrate preference and burrowing behaviour of A. anguilla provides new information about their potential habitat use. Considering that habitat alterations and deteriorations are partly responsible for the decline of the eel, this information can contribute to the development of more effective conservation measures.

Diet-induced phenotypic plasticity in European eel (Anguilla anguilla).

Two phenotypes are present within the European eel population: broad-heads and narrow-heads. The expression of these phenotypes has been linked to several factors, such as diet and differential growth. The exact factors causing this dimorphism, however, are still unknown. In this study, we performed a feeding experiment on glass eels from the moment they start to feed. Eels were either fed a hard diet, which required biting and spinning behavior, or a soft diet, which required suction feeding. We found that the hard feeders develop a broader head and a larger adductor mandibulae region than eels that were fed a soft diet, implying that the hard feeders are capable of larger bite forces. Next to this, soft feeders develop a sharper and narrower head, which could reduce hydrodynamic drag, allowing more rapid strikes towards their prey. Both phenotypes were found in a control group, which were given a combination of both diets. These phenotypes were, however, not as extreme as the hard or the soft feeding group, indicating that some specimens are more likely to consume hard prey and others soft prey, but that they do not selectively eat one of both diets. In conclusion, we found that diet is a major factor influencing head shape in European eel and this ability to specialize in feeding on hard or soft prey could decrease intra-specific competition in European eel populations.

Saving the European Eel: How Morphological Research Can Help in Effective Conservation Management.

The European eel (Anguilla anguilla) is a critically endangered species, whose recruitment stocks have declined to nearly 1% compared to the late 70s. An amalgam of factors is responsible for this, among them migration barriers, pollution, habitat loss, parasite infection, and overfishing. A lot of recent studies focus on aspects that can increase the mature silver eel escapement rate, such as identifying migration barriers and developing passageways or addressing the impact of pollution on the eel's health. However, little attention is given to the eel's morphology in function of management measures. Worryingly, less than 50% of the currently installed management plans reach their goals, strongly indicating that more information is needed about the eel's ecology and behavior. Functional morphological studies provide insights on how species perform behaviors crucial for survival, such as feeding and locomotion, but also in how environmental changes can affect or limit such behaviors. Consequently, functional morphology represents an important biotic component that should be taken into account when making conservation decisions. Hence, here, we provide an overview of studies on the eel's morphology that do not only demonstrate its relation with ecology and behavior, but also provide information for developing and installing proper and more specific management measures.

Built to bite? Differences in cranial morphology and bite performance between narrow- and broad-headed European glass eels.

The presence of two phenotypes in a single species is a widespread phenomenon, also observed in European eel (Anguilla anguilla). This dimorphism has been related to dietary differences in the subadult elver and yellow eel stages, with broad-heads generally feeding on harder and/or larger-bodied prey items than narrow-heads. Nevertheless, both broad- and narrow-headed phenotypes can already be found among glass eels, the stage preceding the elver eel stage. As these glass eels are considered nonfeeding, we investigate here to what degree the observed variation in head width is reflected in variation in the musculoskeletal feeding system, as well as whether this reflects the same variation observed in the older, dimorphic yellow eels. Additionally, we investigate whether musculoskeletal differences between broad- and narrow-headed glass eels have implications on their feeding performance and could thus impact prey preference when eels start feeding. Therefore, we compared the cranial musculoskeletal system of five broad- and narrow-headed glass eels using 3D-reconstructions and simulated the glass eel's bite force using the data of the muscle reconstructions. We found that the variation in the musculoskeletal system of glass eels indeed reflects that of the yellow eels. Broader heads were related to larger jaw muscles, responsible for mouth closure. Accordingly, broad-heads could generate higher bite forces than narrow-headed glass eels. In addition, broader heads were associated with higher coronoid processes and shorter hyomandibulae, beneficial for dealing with higher mechanical loadings and consequently, harder prey. We, thus, show that head width variation in glass eels is related to musculoskeletal differences which, in turn, can affect feeding performance. As such, differences in prey preference can already take place the moment the eels start feeding, potentially leading to the dimorphism observed in the elver and yellow eel stage.

Head shape disparity impacts pollutant accumulation in European eel.

Several aspects of the life cycle of the critically endangered European eel (Anguilla anguilla) remain poorly understood. One such aspect is the broad-versus narrow-head dimorphism, and how this impacts their overall performance at different stages of their life cycle. At the yellow eel stage, the phenotypes show a trophic divergence. We investigated whether pollutant accumulation is affected by this disparity. We show that broad-headed eels contained higher concentrations of mercury and several lipophilic organic pollutants, compared to narrow-headed ones, irrespective of their fat content. The hereby confirmed link between the phenotypic disparity, its associated feeding ecology and its impact on pollutant accumulation thus raises further concerns about their migratory and reproductive success. Considering that pollution is an important contributor to the European eel's decline, our results demonstrate that broad-headed eels are more vulnerable to detrimental pollutant accumulation. This compromises their successful contribution to their population's reproduction and its restoration.

Unimodal head-width distribution of the European eel (Anguilla anguilla L.) from the Zeeschelde does not support disruptive selection.

Since the early 20th century, European eels (Anguilla anguilla L.) have been dichotomously classified into 'narrow' and 'broad' heads. These morphs are mainly considered the result of a differential food choice, with narrow heads feeding primarily on small/soft prey and broad heads on large/hard prey. Yet, such a classification implies that head-width variation follows a bimodal distribution, leading to the assumption of disruptive selection. We investigated the head morphology of 272 eels, caught over three consecutive years (2015-2017) at a single location in the Zeeschelde (Belgium). Based on our results, BIC favored a unimodal distribution, while AIC provided equal support for a unimodal and a bimodal distribution. Notably, visualization of the distributions revealed a strong overlap between the two normal distributions under the bimodal model, likely explaining the ambiguity under AIC. Consequently, it is more likely that head-width variation followed a unimodal distribution, indicating there are no disruptive selection pressures for bimodality in the Zeeschelde. As such, eels could not be divided in two distinct head-width groups. Instead, their head widths showed a continuum of narrow to broad with a normal distribution. This pattern was consistent across all maturation stages studied here.

Using the whole body as a sucker: combining respiration and feeding with an attached lifestyle in hill stream loaches (Balitoridae, Cypriniformes).

Small fishes living in fast-flowing rivers face a harsh environment as they can easily be swept away by the rapid currents. To survive such circumstances, teleosts evolved a wide variety of attachment mechanisms, based on friction, negative pressure or both. Balitorinae (Balitoridae, Cypriniformes) are exceptional in using their whole body as an adhesive apparatus. We investigated the morphological adaptations of Balitorinae by studying the osteology and myology of four species (Beaufortia leveretti, Sewellia lineolata, Pseudogastromyzon myersi, and Gastromyzon punctulatus) using clearing and staining, serial cross-sections and CT-scanning. A kinematic analysis was performed to study the respiration and feeding mechanisms and to identify key structures in these mechanisms. Our research showed that the whole body of Balitorinae acts as a suction disc, with friction-enhancing structures (unculi) on the thickened anterior rays of the paired fins. The abruptly rising head profile, supported by the extremely enlarged lacrimal bone and the flat ventral body surface facilitate effective substrate attachment. During attachment, the pelvic girdle is pulled anterodorsally, suggesting the formation of a negative pressure underneath the body. Detachment by water inflow underneath the body is prevented by three mechanisms. 1) Barbels control the water inflow by detachment and reattachment to the substrate. 2) Most water present underneath the body is removed during inspiration. 3) Excess water is regularly removed by movements of the posterior pectoral fin rays. The balitorine body is thus modified as such that it allows effective attachment, while not impairing respiration. Comparison with other teleosts living in similar environments shows that most species use more locally concentrated modifications of the paired fins and/or the mouth for attachment. The high diversity in teleostean adhesive apparatuses and associated myological modifications suggest a substantial functional convergent evolution, without necessarily highly convergent anatomical adaptations.