Ventilatory and behavioural responses of the marbled sole Pseudopleuronectes yokohamae to progressive hypoxia

This study identified ventilatory and behavioural responses in the marbled sole Pseudopleuronectes yokohamae under experimentally induced progressive decreases in dissolved oxygen (DO) levels. Ventilation frequency showed an increase with decreasing DO levels from normoxia to 2·75 mg O₂ l^?1, followed by a decrease in ventilation frequency at decreased DO levels from 2·00 to 0·75 mg O₂ l^?1. At DO levels below 2·00 mg l^?1, behaviours at the bottom were suppressed, whereas avoidance behaviours increased. A decrease in avoidance behaviours was observed from 1·00 to 0·75 mg O₂ l^?1. Upside‐down reversal and incapacitation at DO levels of 1·00–0·75 mg O₂ l^?1 suggested that sublethal effects on P. yokohamae were induced. The responses observed before the sublethal DO level could be interpreted as an effort to maintain oxygen uptake, reduce routine activities and facilitate avoidance. The observed DO level thresholds that induce behavioural responses, in addition to sublethal effects, indicate hypoxia‐tolerance that is important for understanding the effects of hypoxia on coastal ecosystems.     

Comparison between the life cycles of two Soleidae, the common sole, Solea solea, and the thickback sole, Microchirus variegatus, in the Bay of Biscay (France)

The life history of two Soleidae, the common sole, Solea solea, and the thickback sole, Microchirus variegatus, were compared in the Bay of Biscay in an attempt to set out factors which could explain settlement styles known to be different between juveniles of each species. Common sole juveniles had been shown to depend on coastal and estuarine nurseries, and the thickback sole to develop in open-sea nurseries, although the spawning grounds and spawning season of both species overlapped (offshore and at springtime, respectively). For this study, data on adult, juvenile and larva distributions were obtained from cruises carried out in the Bay of Biscay during the last decade. In addition, growth rate of larvae and planktonic interval duration, estimated by means of otolith increment analysis, were compared, as well as literature-derived information on behaviour of larvae. By comparing larval features, it appeared that thickback sole did not obtain the advantage of a slightly longer pelagic life span for an increased dispersal, due to an early shift to benthic behaviour. Other evidence was given by more specifically stated distributions that the further and deeper offshore spawning of M. variegatus, compared to S. solea, was a likely key-factor of the juvenile settlement process. This could explain why the thickback sole, contrary to the common sole, never reach coastal areas and thus settle offshore, in waters deeper than 30 m.     

The influence of prey size,sediment thickness and fish size on consumption in common sole (Solea solea L.)

This study determined prey consumption in common sole as a function of prey size (0–0.5, 1–1.5, 2–2.5 and 4–5 g), sediment thickness (20 cm and 2 cm) and fish size (50 g, 125 g or 300 g). Prey consumption (in numbers of prey eaten per fish per day) was reduced with increasing prey size and sediment thickness, and was increased with increasing fish size (p < .001 for all factors). All 3 factors showed significant two way interactions (p < .001) when expressed in numbers of prey eaten. Prey consumption decreased with prey size when prey could not escape by burying (2 cm of sediment thickness) irrespective of fish size. We suggest that increasing effort to ingest and handle larger prey played a role. Prey consumption increased with fish size when prey could not bury (2 cm of sediment thickness). However, when prey was able to bury (at 20 cm sediment thickness) prey consumption was similar irrespective of fish size (p < .001 for interaction fish size × sediment). This interaction suggests that with increasing fish size there is an increasing mismatch between foraging adaptation and prey burial depth. This may explain the dominance of crustaceans in the diet of adult common sole in nature, despite the high abundance of polychaetes.     

Micro‐anatomical characterization of vertebral curvatures in Senegalese sole Solea senegalensis

The micro‐anatomical changes associated with lordotic and kyphotic vertebral curvatures (VC) in juvenile and adult Senegalese sole Solea senegalensis are described. In addition, it is demonstrated that the tissue and cellular structures of individual vertebrae can be severely affected. Two main conformations were found in deformed juvenile specimens: flattened vertebrae with dorso‐ventral compression and trapezoidal vertebrae forming concave and convex sides under compressive and tensile stresses. Histological analyses revealed the occurrence of an ectopic cartilaginous tissue within the acellular bone, both in juveniles and adults, possibly to cope with altered mechanical stress in deformed vertebrae. The results suggest that the alteration in loading to which curved vertebral columns are subjected might trigger vertebral reshaping and differentiation of cells towards this ectopic tissue. In addition, mesenchymal cells appear to play an important role in its formation. It is here proposed that the acellular bone of S. senegalensis is capable of adaptively responding to altered loading regimes at the structural level by reshaping vertebrae and at the micro‐anatomical level by recruiting chondrocyte‐like cells to areas of altered mechanical stress.     

The mode of hatching of the monogenean Entobdella soleae, a skin parasite of the common sole (Solea solea).

Observations have been made on the hatching behaviour of the larva of the monogenean Entobdella soleae and on the effects of various enzymes on the opercular cement of the egg. These observations indicate that hatching is brought about by a proteolytic hatching fluid which is produced by two pairs of ventral head glands and spread over the inner surface of the opercular joint by rotation of the larva about its longitudinal axis. After hatching there is no trace of the ventral head glands. Similar glands are present before hatching in the oncomiracidium of E. hippoglossi.     

Spatial variability in digenean metacercariae infection of 0-group common sole Solea solea among nurseries along the French Atlantic coast

We sampled 0-group sole juveniles (N = 174) in September and October 2003 in 9 major nurseries located along the French Atlantic coast (English Channel and Bay of Biscay). 0-group sole were infected with 3 genera of digenean metacercariae, Timoniella spp. (Acanthostomidae), Prosorhynchus crucibulum and Prosorhynchus sp. A (Bucephalidae), Podocotyle sp. (Opecoelidae), and an unidentified species of Digenea. Parasite infection levels in the English Channel nurseries were lower, and the community composition was different from Bay of Biscay nurseries. We hypothesize that the difference between geographic areas was due to differences in first intermediate host communities and, to a lesser extent, because of lower temperatures in the English Channel compared to the Bay of Biscay. For the Bay of Biscay nurseries, mean total parasite abundance was strongly negatively correlated with mean annual river flow. This relationship may be the result of the more upstream location of 0-group sole nurseries in estuaries so that fish were further from local points of parasite transmission than those in embayed nurseries. Digenean metacercariae load may be influenced by 3 major local factors, i.e. abundance and proximity of the first intermediate hosts and cercariae dispersal capacities.     

Characterizing the escape response of juvenile summer flounder Paralichthys dentatus to diel‐cycling hypoxia

Swimming speed, angular correlation and expected displacement were measured in juvenile summer flounder Paralichthys dentatus acclimated to either oxygen saturation (c. 7·8 mg O₂ l^?1; saturation‐acclimated fish) or diel‐cycling hypoxia (cycling between 11·0 and 2·0 mg O₂ l^?1) for 10 days and subsequently exposed to more severe diel‐cycling hypoxia (cycling between 7·0 and 0·4 mg O₂ l^?1). Saturation‐acclimated P. dentatus exhibited an active response to declining dissolved oxygen (DO) by increasing swimming speed, angular correlation and expected displacement to peak levels at 1·4 mg O₂ l^?1 that were 3·5, 5·5 and 4·2 fold, respectively, greater than those at DO saturation. Diel‐cycling hypoxia‐acclimated P. dentatus also exhibited an active response to declining DO, although it was relatively less pronounced. Diel‐cycling hypoxia‐acclimated P. dentatus swimming speed, however, still doubled as DO decreased from 7·0 to 2·8 mg O₂ l^?1. Diel‐cycling hypoxia‐acclimated P. dentatus did not recover as well from low DO exposure as did saturation‐acclimated fish. This was reflected in their relatively more random swimming (low angular correlation between successive moves) and poor maintenance of rank order between individuals during the recovery phase. Even saturation‐acclimated P. dentatus did not resume swimming at speeds observed at saturation until DO was 4·2 mg O₂ l^?1. Paralichthys dentatus were very sensitive to decreasing DO, even at DO levels that were not lethal or growth limiting. This sensitivity and their poor recovery may preclude juvenile P. dentatus from using highly productive nursery habitats affected by diel‐cycling hypoxia.     

Interaction between exopolysaccharide and oxygenation levels on habitat selection in the sole Solea solea (L.)

A habitat selection experiment was conducted to examine the behavioural response of sole Solea solea to a combination of sediment quality (exopolysaccharides, EPS-free, i.e. 0 mg l⁻¹ and EPS-rich, i.e. 4 mg l⁻¹) and water oxygenation level (100 and 35% air saturation). The distribution of sole was influenced differently by the type of substratum depending on the water oxygenation level. In normoxia, sole settled preferentially on sand whereas under hypoxic conditions, sole settled preferentially on the muddy substratum. In order to explain these apparently counter-intuitive observations, it is proposed that, via cutaneous respiration, young sole are able to take advantage of the large quantities of oxygen produced by microphytobenthic organisms present in the upper few millimetres of muddy substratum.     

The relationships between fish size and otolith dimensions in the common sole (Solea solea (Linnaeus, 1758)) captured in the Northeastern Mediterranean

Fish specimens were captured by a commercial bottom trawler at a depth of 50–80 m from Iskenderun Bay (Hatay, Turkey) between December 2017 and May 2018. The bottom trawl gear used was equipped with a 44 mm stretched mesh size net at the cod-end. Blind side and eyed side otolith lengths (OL), otolith breadths (OB) and otolith weights (OW) were measured from each specimen to the nearest 0.001 mm and 0.0001g respectively. A total of 110 fish (43 females and 67 males) were collected. Total length ranged from 20.8 to 28.2 cm and 68.0 to 166.1 g (males) and 21.1 to −28.5 cm and 74.5 to 201.4 g (females). The coefficients of determination between fish weight and otolith weight, and total length and otolith weight (sexes combined) were found as R² = .7694 (0.77) and R² = .6274 (0.63), respectively. A moderate positive relationship between the total length-otolith dimensions, and fish weight-otolith dimensions, was also demonstrated.     

Bio‐energetics underpins the spatial response of North Sea plaice (Pleuronectes platessa L.) and sole (Solea solea L.) to climate change

Climate change is currently one of the main driving forces behind changes in species distributions, and understanding the mechanisms that underpin macroecological patterns is necessary for a more predictive science. Warming sea water temperatures are expected to drive changes in ectothermic marine species ranges due to their thermal tolerance levels. Here, we develop a mechanistic tool to predict size‐ and season‐specific distributions based on the physiology of the species and the temperature and food conditions in the sea. The effects of climate conditions on physiological‐based habitat utilization was then examined for different size‐classes of two commercially important fish species in the North Sea, plaice, Pleuronectes platessa, and sole, Solea solea. The two species provide an attractive comparison as they differ in their physiology (e.g. preferred temperature range). Combining dynamic energy budget (DEB) models with the temperature and food conditions estimated by an ecosystem model (ERSEM), allowed spatial differences in potential growth (as a proxy for habitat quality) to be estimated for 2 years with contrasting temperature and food conditions. The resulting habitat quality maps were in broad agreement with observed ontogenetic and seasonal changes in distribution as well as with the recent changes in distribution which could be attributed to an increase in coastal temperatures. Our physiological‐based model provides a powerful tool to explore the effect of climate change on the spatio‐temporal fish dynamics, predict effects of local or broad‐scale environmental changes and provide a physiological basis for observed changes in species distributions.     

Salinity effects on behavioural response to hypoxia in the non-native Mayan cichlid Cichlasoma urophthalmus from Florida Everglades wetlands

This study quantified the hypoxia tolerance of the Mayan cichlid Cichlasoma urophthalmus over a range of salinities. The species was very tolerant of hypoxia, using aquatic surface respiration (ASR) and buccal bubble holding when oxygen tensions dropped to <20 mmHg ( c. 1·0 mg l⁻¹) and 6 mmHg, respectively. Salinity had little effect on the hypoxia tolerance of C. urophthalmus , except that bubble holding was more frequent at the higher salinities tested. Levels of aggression were greatest at the highest salinity. The ASR thresholds of C. urophthalmus were similar to native centrarchid sunfishes from the Everglades, however, aggression levels for C. uropthalmus were markedly higher.     

The effect of hypoxia on locomotor performance and behaviour during escape in Liza aurata

Escape performance was investigated in the golden grey mullet Liza aurata exposed to various levels of oxygen: >85 ( i.e. normoxia), 50, 20 and 10 % air saturation. Since the golden grey mullet performed aquatic surface respiration when air saturation approached 15–10 %, escape performance was tested at 10 % air saturation with and without access to the surface (10 % S and 10 % C, respectively). Various locomotor and behavioural variables were measured, such as cumulative distance, maximum swimming speed, acceleration, responsiveness (per cent of responding fish), response latency and directionality. Golden grey mullet showed a decrease in responsiveness when the oxygen level was reduced to 10 % air saturation, whether the surface access was obstructed or not. Hypoxia did not have any effect on the response latency. Cumulative distance and maximum swimming speed over a fixed time were significantly different between normoxic conditions and 10 % C, while no differences were found in maximum acceleration. While the fish's 'C‐bend' was mainly directed away from the stimulus in normoxia, the proportion of away and towards 'C‐bend' was random when the oxygen was ≤20 % air saturation. This suggested an impairment of the left‐right discrimination at the initiation of the fast start. Hypoxia affected golden grey mullet escape performance mainly through an impairment of responsiveness and directionality, while locomotor performance was affected only in severe hypoxia when the surface was obstructed. The study showed that, in addition to forcing the fish to the surface as shown by previous studies, hypoxia may also reduce fish elusiveness facing a predator by directly impairing its escape performance.     

Isolation of polymorphic DNA microsatellites in the common sole Solea vulgaris

A microsatellite‐enriched genomic library was obtained from the common sole, Solea vulgaris, and seven polymorphic dinucleotide markers were successfully optimized. These markers showed levels of expected heterozygosity ranging from 0.55 to 0.83 and allele number ranging from eight to 12. Three of these markers were also found to successfully amplify in the closely related Solea senegalensis and can be employed to define population genetic structure of the two Solea species and for inferring stock origins.     

The influence of sand on the estimation of resting metabolic rate of juvenile sole, Solea solea (L.)

The influence of a sandy substrate on the estimation of the resting metabolic rate of juvenile sole was determined using a static type of respirometer. Oxygen consumption of fish deprived of sand was almost double that of fish provided with sand.     

High dietary arachidonic acid levels affect the process of eye migration and head shape in pseudoalbino Senegalese sole Solea senegalensis early juveniles

The effect of high dietary levels of arachidonic acid (ARA) on the eye migration and cranial bone remodelling processes in Senegalese sole Solea senegalensis early juveniles (age: 50 days post hatch) was evaluated by means of geometric morphometric analysis and alizarin red staining of cranial skeletal elements. The incidence of normally pigmented fish fed the control diet was 99·1 ± 0·3% (mean ± s.e .), whereas it was only 18·7 ± 7·5% for those fed high levels of ARA (ARA‐H). The frequency of cranial deformities was significantly higher in fish fed ARA‐H (95·1 ± 1·5%) than in those fed the control diet (1·9 ± 1·9%). Cranial deformities were significantly and negatively correlated with the incidence of normally pigmented animals (r² = ?0·88, P < 0·001, n = 16). Thus, fish displaying pigmentary disorders differed in the position of their eyes with regard to the vertebral column and mouth axes, and by the interocular distance and head height, which were shorter than in fish not displaying pigmentary disorders. In addition to changes in the positioning of both eyes, pseudoalbino fish showed some ARA‐induced osteological differences for some of the skeletal elements from the splanchnocranium (e.g. right premaxillary, dentary, angular, lacrimal, ceratohyal and branchiostegal rays) and neurocranium (e.g. sphenotic, left lateral ethmoid and left frontal) by comparison to normally pigmented specimens. Pseudoalbino fish also had teeth in both lower and upper jaws. This is the first study in Pleuronectiformes that describes impaired metamorphic relocation of the ocular side eye, the right eye in the case of S. senegalensis, whereas the left eye migrated into the ocular side almost normally.     

Dietary inclusion of mussel meal enhances performance and improves feed and protein utilization in common sole (Solea solea,Linnaeus, 1758) juveniles

The present study was carried out to test different mussel meal (MM) dietary levels in combination with fishmeal (FM) on the growth performance, fatty acid composition and liver histology of common sole, Solea solea juveniles to highlight the growth potential of this species. Four isoproteic (53%) and isolipidic (11%) pelletized diets were formulated to contain graded levels of mussel meal, MM0 (0%), MM25 (25%), MM50 (50%) and MM75 (75%), up to 75%. Sole juveniles (initial individual mean body weight 13.1 ± 2.3 g, n = 840) were fed to satiation for 91 days. Seventy fish per tank (500‐L, 0.64 m² bottom surface) were reared in 12 tanks (3 tanks per treatment) at 20 ± 1°C. Diets containing MM (MM25, MM50 and MM75) gave a significantly higher specific growth rate (SGR, 1.27 ± 0.01, 1.38 ± 0.06 and 1.40 ± 0.05, respectively), higher feed intake and lower feed conversion rate (FCR, 1.09 ± 0.01, 1.00 ± 0.04 and 0.98 ± 0.02, respectively) when compared to the FM‐based diet (MM0, SGR, 0.98 ± 0.11, FCR, 1.52 ± 0.13). Carcass proximate composition was not influenced by dietary treatments, with the exception of the significantly lower lipid content in the MM75 group. Protein efficiency ratio (PER) and gross protein efficiency (GPE) were significantly improved by the mussel meal inclusion (PER, 1.29 ± 0.12, 1.76 ± 0.01, 1.89 ± 0.06, 1.95 ± 0.08; GPE, 25.29 ± 1.85, 33.38 ± 0.89, 35.96 ± 1.36, 36.59 ± 1.05 in MM0, MM25, MM50 and MM75, respectively). A significant decrease in the viscerosomatic index was observed in fish fed with MM50 and MM75 in comparison to MM0. The hepatosomatic index of fish fed with MM0 and MM25 was higher than that of fish fed with MM75, although the histological examination of liver parenchyma in all experimental groups showed a uniformly abundant accumulation of lipid droplets. Carcass fatty acid composition was significantly affected by dietary treatments, reflecting the dietary fatty acid profile. According to these results, the inclusion of MM in experimental FM‐based diets improved the performance and feed utilization of common sole juveniles. The inclusion of MM in the present trial allowed a higher SGR than that registered in previous growth trials on common sole. This study could provide useful information to detect effective ingredients for practical diets in Solea solea. It also seems advisable to consider an inclusion of at least 25% MM in the experimental reference diet to be used for further application towards the development of specific diets for this species.