Parasite fauna and community structure of bathydemersal fishes: notacanthus bonaparte (osteichthyes), etmopterus spinax and deania profundorum (chondrichthyes)

• Autores: Wolf Isbert
• Directores de la Tesis: Francisco Esteban Montero Royo (dir. tes.), Ana Pérez del Olmo (codir. tes.), Maite Carrassón López de Letona (codir. tes.)
• Lectura: En la Universitat de València ( España ) en 2017
• Idioma: español
• Tribunal Calificador de la Tesis: Pablo Abaunza (presid.), Mercedes Fernández Martínez (secret.), Paolo Merella (voc.)
• Materias:
  • Ciencias de la vida
• Texto completo no disponible (Saber más ...)
• Resumen

  • The deep-sea is the largest biome on earth, but it is also still the less studied (Ramirez-Llodra et al. 2010). While in former times the deep-sea was considered as highly ‘stable’ with low variations below the permanent thermocline, more recent research clearly indicates to a more dynamic environment (Gage 2003, Ramirez-Llodra et al. 2010). Natural effects exerted on deep-sea habitats arise from different factors which comprise e.g. the horizontal movement of huge water masses driven by circum-global currents, which can change salinity and temperature regimes. Additionally, topographic underwater features such as seamounts and canyons interact with these currents and create environmental conditions distinctly different to the continental slope or deep-sea plains, which can enhance the food supply and diversity in the deep-sea on a local scale (Levin & Dayton 2009 and references therein). Therefore, the high spatial heterogeneity of deep-sea habitats together with the spatial and temporal limitations of food supply in their communities (Snelgrove & Grassle 1995) can result in a high variability of the diversity, even in very small spatial scales (Levin & Dayton 2009).

    The current knowledge on these deep-sea dynamics and its habitats is still scarce and negligible when compared to the knowledge ofcostal and shallow water ecosystems (RamirezLlodra et al. 2010, Snelgrove et al. 2016). This applies also to the deep-sea fishes for which knowledge is often limited to species of commercial value and targeted in specific areas (Snelgrove et al. 2016). Therefore, based on this unbalanced study effort, it is recommended to consider assumptions about common patterns in the deep-sea with caution (Snelgrove et al. 2016). The scant overall information lacks knowledge on several ecological and biological traits of deep-sea fishes, including their parasites. Several aspects of parasites, such as their life cycles and distribution patterns in the deep-sea are often assumed based on the knowledge from shallow water fishes. The few data available on parasites in deep-sea fishes show similarities to shallow waters, where a certain relation between parasite communities and host related factors exists. Parasite life cycles in the deepsea ecosystems are often not known. Available studies show that the diversity of certain parasite groups seems to be distinctly lower compared to shallow waters (Klimpel et al. 2009). This lower diversity is partly explained in some higher taxa, such as Digenea, by the fact that few parasites followed and co-evoluted with their hosts in the deep. Further, a lower host density in the deep-sea and the inappropriate life cycles may impede a successful colonization of this habitat (Campbell et al. 1980, Bray et al. 1999, Klimpel et al. 2006). Increasing knowledge on fish parasite communities from the deep-sea would not only provide more data on the parasites, but even indicate to host related ecological and biological traits, as parasites can be used as biological indicators. This would also provide an insight in the transmission pathways of parasites in extreme environments with often lower host diversity and density (Leung et al. 2015).

    In particular, the use of parasites as biological indicators is recommended for rare species or species difficult to sample (MacKenzie & Abaunza 1998), which is partly the case for the three species studied in this work: Notacanthusbonaparte Risso, 1840 (Notacanthiformes: Notacanthidae), Etmopterus spinax L., 1758 (Squaliformes: Etmopteridae), and Deania profundorum Smith & Radcliffe, 1912 (Squaliformes: Centrophoridae).

    The data available for deep-sea habitats and their fish fauna clearly indicate to life history traits with slow growth, late maturity and low fecundity which make deep-sea fishes less resilient to anthropogenic impacts such as fisheries (Koslow et al. 2000, Bergstad et al. 2013). This also applies to the three species studied here, and although all have a low or no commercial value, they suffer fishery impacts due to partly high by-catch mortalities. Notacanthus bonaparte is ‘grazing’ on benthic fauna and in some areas may exhibit high abundances. However, the particular role of N. bonaparte in ecosystems is not known, and it can only be speculated if a depletion would have cascading effects in the ecosystem. Regarding the shark species (E. spinax and D. profundorum), their role/importance in deep-sea ecosystem is not clear but as predators of higher trophic levels (Cortés 1999) it is suggested, that their depletion or extinction could have profound consequences for the local community and ecosystem stability.

    The specific objectives of this work are: 1. To contribute to the knowledge on the parasite fauna of the three selected species N. bonaparte, E. spinax y D. profundorum.

    2. To describe species new to science.

    3. To describe the parasite communities of N. bonaparte, E. spinax and D. profundorum.

    4. To generate information on the composition and abundance of parasite species which may be used as potential indicators.

    5. To analyse potential relationships between the detected parasite communities with the diet and trophic ecology of the host.

    Annotated checklist of parasites recorded from the species of the three families of deep-sea fish: Centrophoridae, Etmopteridae and Notacanthidae A compilation of data currently available on recorded parasites for the three host families (Centrophoridae, Etmopteridae and Notacanthidae) which comprise the three model species, has been performed (Table 4.1). A thorough literature search has been conducted consulting different databases (e.g. Google Scholar, Web of Knowledge, World of Copepods, Global Cestode Database and Host-parasite database of the Natural History Museum, London), but also the comprehensive checklist compiled by Klimpel et al. (2009). The information found by means of a web search engine, was verified with the original source (publication) when available.

    All three fish families exhibited a different number of valid species, where some species are still under discussion. The total number of valid fish species (82) is distributed over these three families as follows: 20 centrophorids, 51 etmopterids and 11 notacanthids. The found publications dealing with parasites species described in these host families are low in number compared to shallow water or commercially important species, but an increasing study effort is observable since the 70’s (Fig. 4.1). Further, the publications reveal a clear geographical bias with most studies conducted in the Northeast Atlantic followed by the Northwest Atlantic, the Southwest Pacific, and the Mediterranean Sea.

    Several families of different parasite higher taxa groups were found with varying importance with respect to elasmobranchs and teleost hosts. These taxa were: Cestoda, Monogenea, Trematoda (Digenea), Nematoda, Copepoda, Isopoda, Cirripedia and Amphipoda (Fig. 4.2). In both elasmobranch species most parasites recorded were assigned to the cestodes followed by the copepods, while in Notacanthidae digeneans were the most diverse group followed by monogeneans. These are patterns which were already observed for other elasmobranchs and osteichthyes (Campbell et all. 1980, Cribb et al. 2002, Caira & Healy 2004). Amphipods and cirripeds were detected in etmopterids only (Fig. 4.4, 4.5). The lower overall diversity in monogeneans may hint to sampling artefacts or a general low presence in the deep-sea as previously suggested (De Buron & Morand 2004). The parasite taxa detected in these fish families partly represent families which were already found frequently in other fishes from the deepsea (Fig. 4.3). The proportions between specialist and generalist species of all parasite groups were different between all three fish families, where the notacanthids showed the highest proportion of specialist species (almost 58%) followed by etmopterids (50%) and centrophorids (30%) (Fig. 4.6). Specialists were not only found among monogeneans, but also digeneans (in Notacanthidae) and cestodes (both in elasmobranchs). As previously suggested, generalist feeders may be infected by a more diverse parasite fauna with more generalist species (Klimpel et al. 2006, Chambers 2008); the differences between the fish families are partly explained by the different feeding habits with often broader ranges of prey items in sharks. In comparison notacanthids show a more limited range of prey items and are partly highly specialised. The proportions of heteroxenous and monoxenous parasite taxa were similar for all three families; the highest proportion of heteroxenous parasites was detected in notacanthids, probably in part due to their strict benthic diet. In etmopterids, monoxenous parasite taxa had a higher contribution, in part owing to two taxa found exclusively in this fish family. This might also be related to the higher proportion of adult parasite stages recorded for etmopterids, while in centrophorids the proportion is almost balanced. In etmopterids, more monoxenous species were recorded which mostly infect their host as adult stage (except e.g. Gnathiidae). The high proportion of adults in notacanthids is mainly represented by digeneans which may hint to its specialised, benthic feeding habit. Interestingly the high amount of larval stages in centrophorids, which is the family with largest body sizes of all three fish families, indicates to an important role as intermediate or at least paratenic host. Consequently, predators of these species, having at least the same size of these sharks, might exist in their habitats. Though, further studies are needed to analyse whether some larval cestodes may occur only in smaller, younger sharks and diminish in adults.

    A new species of Tinrovia Mamaev, 1987 (Monogenea: Microcotylidae) from the deep-sea fish Notacanthus bonaparte Risso (Notacanthiformes: Notacanthidae) in the western Mediterranean and the Northeast Atlantic During the analysis of the parasite communities from the shortfin spiny eel, Notacanthusbonaparte Risso, 1840, a new monogenean species was detected and described. The parasite fauna of the deep-sea fish N. bonaparte is poorly studied and to date only two species have been described: the trematode Steringovermes notacanthi Bray, 2004 and the cestode Bathycestus brayi Kuchta & Scholz, 2004. This new microcotylid, Tinrovia mamaevi n. sp. (Monogenea: Polyopisthocotylea), is described from the gills of 165 specimens sampled in the western Mediterranean and Northeast Atlantic. The obtained specimens were used for a detailed morphological study by means of light and confocal laser scanning microscopy. The morphological traits observed in the analysed monogenean specimens from both areas justify their classification belonging to the same species. This species is allocated to the subfamily Syncoelicotylinae Mamaev & Zubchenko 1978 due to the possession of a symmetrical haptor with two separate frills. This species is assigned to the genus Tinrovia which includes the type- and only other species T. papiliocauda Mamaev, 1987. Tinrovia mamaevi differs from T. papiliocauda, in having a narrower haptor with a lower number of clamps. Clamps are also smaller in the new species, testes more numerous, the genital atrium smaller with a lower number of spines, and the eggs have a short and a long filament (Table 5.1). The clamps in T. mamaevi n. sp. are of the ‘microcotylid’ type, arranged in two distinct lateral haptoral frills (Fig. 5.1). Previous publications suggested that clamps of Syncoelicotylinae have to be considered ‘massive’ (Mamaev & Zubchenko 1978, Mamaev 1987, Mamaev & Brashovian 1989) however,clamps of T. mamaevi were slightly smaller than in T. papiliocauda, especially their sclerites were slender and more delicate. Therefore, in these cases descriptions could be ambiguous and should be referred to total clamp size in relation to the body size or to the relative sizes of the sclerites. This applies also to the description of the haptor made for two species of Syncoelicotylinae. In the present study we could observe an overall smaller haptor in T. mamaevi compared to T. papiliocauda, and the lateral frills appear to be relatively smaller and narrower. In the generic diagnoses of two species of the genera, Syncoelicotyle and Tinrovia, the haptor is described as ‘butterfly-shaped’, meaning wide, separated haptor frills (Mamaev & Zubchenko 1978, Mamaev 1987) (Figs. 5.1, 5.2). We suggest that this description in the diagnoses of these species of Syncoelicotylinae can be controversial. Firstly, we observed overall narrower lateral frills suggesting the wide shape as no longer valid for diagnostic of this genus. Secondly, we suggest using a more generic term to refer to characters such as ‘wide haptor frill’, as descriptions referring to peculiar shapes can be misinterpreted depending on the observer. Along with the lower spine number, the genital atrium in T. mamaevi is smaller and exhibits a different pattern of armed muscular pads compared to the genital organ described for T. papiliocauda. However, owing to the difficulties describing complex traits the supposedly different genital atrium lobulation should be interpreted with caution. The here applied confocal techniques were highly useful to interpret especially the 3D- structure of the genital atrium (Fig. 5.3). The use can help to diminish controversies about the correct interpretation of traits and enhance the reliability for diagnostics. In the present study, eggs also differed to the diagnosis of the genus (two short filaments); and branched caeca, usually described as anastomosed, could not be observed due to dense vitelline follicles. The description of these characters are known to be controversial in other polyopisthocotyleans, therefore both morphological traits are unreliable for taxonomical diagnoses. We suggest an emended diagnosis of the genus Tinrovia: as in Mamaev (1987) except for: Haptor with two lateral frills not joining posteriorly, markedly winged when frills wide; eggs with two filaments (short or long).

    Dichelyne (Cucullanellus) romani n. sp. (Nematoda: Cucullanidae) in notacanthid fishes from the Northeast Atlantic and western Mediterranean A new nematode, Dichelyne (Cucullanellus) romani n. sp. (Nematoda: Cucullanidae), is described from the digestive tract of two notacanthid fishes, Notacanthus chemnitzii Bloch, 1788 and N. bonaparte Risso, 1840 (Notacanthiformes: Notacanthidae), from the Northeast Atlantic Ocean and western Mediterranean Sea. Currently, the helminth fauna of both notacanthids is poorly studied and to date one cucullanid nematode has been detected in N. chemnitzii, while for N. bonaparte no nematode record exists (Gibson et al. 2005, Soares 2007). This is the first species of Dichelyne Jägerskiöld, 1902 in a notacanthid fish and one of the only two records in deep-sea fish species, and the fourth Dichelyne (Cucullanellus) species described for the Mediterranean Sea. A detailed morphological study of these specimens was performed by means of light and scanning electron microscopy. The individuals of this nematode species possess a precloacal sucker, ten pairs of caudal papillae, and an intestinal caecum, typical features for species belonging to Dichelyne (Cucullanellus) (Figs. 6.1–6.3). The new species differs from other members of this subgenus, recorded in other fish species from different geographical areas including the Atlantic Ocean and the Mediterranean Sea, in different morphological traits. The new species has a larger body size, smaller spicule/body length ratio, and differs in the position of deirids and excretory pore, and in the distribution of caudal papillae (Table 6.1). Interestingly, in the present study, specimens taken from the Mediterranean Sea were smaller than from the Atlantic Ocean and additionally males found in N. bonaparte had a smaller body size than male specimens obtained from N. chemnitzii, both hosts from the Atlantic Ocean. Despite the biometric differences, nematode specimens from both hosts and areas were considered to belong to the same species because most body ratios and other values were identical among them. These here detected differences in the nematode development agree with other studies and supposedly are related to different biological and environmental factors such as host species, host size and condition, and temperature (Sasal et al. 2000, Timi et al. 2009). Considering previous publications of differences in fish sizes between the Northeast Atlantic Ocean and the Mediterranean Sea (Stefanescu et al. 1992) it is supposed that the lower host body size of N. bonaparte from the latter area affects the size of these nematodes (Poulin 1998). In the present study we could also observe a broad intraspecific variability in certain aspects of the morphological traits, in particular considering the presence/absence of the intestinal caecum and the distribution of the papillae in the caudal region of the males. The latter trait is one of the key diagnostic features to identify species of this subgenus. Cases of high intraspecific variability in these morphological traits were also detected in other Dichelyne spp. (De & Maity 1995, Li et al. 2014). The differences in the distribution of papillae recorded in the present study were partly detected on the same specimen (both sides of the tail) (Fig 6.1J, K). Along with differences which might be related to the fixation procedure or the examination of material from fresh or frozen hosts, in this case we suggest simple intraspecific variabilities which seem to occur quite frequently. The revision of the described species for Dichelyne (Cucullanellus) spp. revealed many uncertainties of their validity and a profound revision would be necessary, especially when considering the morphological variabilities observed here and elsewhere.

    Seasonal variation of parasite communities of Notacanthus bonaparte Risso, 1840 Notacanthiformes: Notacanthidae) over the Northwest Mediterranean slope The short-fin spiny eel Notacanthus bonaparte Risso, 1840 was first described from the Western basin of the Mediterranean Sea, and its distribution extends to the Northeast Atlantic (Froese & Pauly 2017). Few studies exist on this species and available data comprise its spatial and depth-related distribution, reproduction and diet (e.g. Stefanescu et al. 1992, Coggan et al. 1998, Rodríguez-Romeu et al. 2016). The aim of this study is to provide detailed information on the parasite communities of N. bonaparte from different seasons and depth ranges of the slope in the western Mediterranean. Further, we want to assess the potential effects on the parasite communities imposed by the factors depth, season, host size and sex, trying to detect links between environmental parameters from this area and the parasite communities. The analyses were performed on the parasite communities of 150 specimens of N. bonaparte sampled in the western Mediterranean Sea (Balearic Sea, Spain) from three bathymetric strata between 600 and 2,000 m over the seasons in 2007/08 and 2011 (Fig. 7.1). The depth was separated in three depth strata: 600–1,000 (D1), 1,000–1,400 (D2) and 1,400–1,800 (D3). Each depth range was joined with the season (winter (W), spring (Sp), summer (S), autumn (A)) of sampling (Table 7.1). The potential effects by these ‘DepthSeason’ combinations on the parasite communities and on single parasites were tested including also the cofactors sex and status of maturity (fish size). We tested the effect of ‘DepthSeason’ combinations with co factors (fish size, sex) on parasite infracommunity parameters, such as richness and diversity, and on the abundance and prevalence of single parasite species (common species prevalence >5%). Latter analyses were repeated using samples from different depth strata where samples were taken in a particular season (D1 and D2, summer; D1–D3, autumn). Seasonal variation in prevalence and abundance were tested for D1, where samples from all seasons were available, including also the cofactors. The potential effect on parasite community composition and structure was assessed considering the factor ‘DepthSeason’, or ‘season’ and ‘depth’ separately. Finally, the potential impact of environmental variables (temperature, salinity, oxygen, turbidity) imposed on the parasite communities was tested. Overall, parasite communities of N. bonaparte in this area are poor, especially when considering its benthic feeding habit, supposedly exposed to the many benthic parasite life cycles. Almost all analysed N. bonaparte specimens were infected by at least one parasite species (overall prevalence 94.7%), while the overall mean abundance was 94.3±112.6. The infracommunity composition is defined by the factors, depth, maturity status (size) and sex. The infracommunity richness and Margalef Species Richness revealed significant differences between ‘DepthSeason’ combinations, where samples taken in spring showed a higher richness (Table 7.2). Margalef Species Richness and Brillouin’s diversity were significantly different between sexes, where mean values for both indices were significantly higher in males. We detected five taxa, all of them recorded for the first time in N. bonaparte (Table 7.3): a larval cucullanid which could not be identified to species level, the monogenean Tinrovia mamaevi and the nematode Dichelyne (Cucullanellus) romani; the other two taxa were larval stages of Hysterothylacium aduncum and Tetraphyllidea fam. gen. sp. and showed overall prevalences below 5%, supposedly being accidental infections. The parasite D. (C.) romani did not show any pattern considering any of the tested factors. In contrast, the most abundant taxon, the cucullanid larva, showed significant differences between ‘DepthSeasons’ and between depths, fish size and sex. This parasite seems to be accumulated during host life showing higher abundances in larger fish of deeper waters (on the middle and lower slope) and is more abundant in larger sized females. The monogenean T. mamaevi was recorded in the upper slope mainly during the spring season. The abundance of this parasite differed significantly among all ‘DepthSeason’ combinations with highest values in D1, but without any effect by fish size or sex. Abundance and prevalence of this monogenean were significantly different between the four seasons from D1. The prevalence for spring was significantly higher compared to summer and autumn. Both taxa were slightly related to measured environmental parameters: cucullanid larvae to turbidity and T. mamaevi to temperature and salinity (Fig. 7.2).

    Communities were richer in shallower waters (D1) owing to the presence of T. mamaevi and both uncommon taxa, H. aduncum and Tetraphyllidea gen. sp., while cucullanid larvae showed lower abundances. Higher abundances of cucullanid larvae were detected in larger mature specimens, indicating an accumulation of this parasite during host growth. Further, females showed higher abundances of this parasite which can be explained by their larger sizes, compared to males. The lower abundance in males might partly explain the higher Margalef Species Richness and Brillouin diversity indices calculated in males. Although not for the present study, a bigger-deeper trend for this species has been reported (Coggan et al. 1998, Rodríguez-Romeu et al. 2016), which also explains the higher abundances of this nematode observed in deeper waters. We suggest that 3rd stage larvae of this cucullanid nematode are free-living, which has been observed for another cucullanid (Køie 2000), and after hatching they sink to the bottom and survive a certain period in the sediment. As sediment has been recorded in stomach (Rodríguez-Romeu et al. 2016), we argue that cucullanid larvae can infect fish when they are ingested with sediments or while fish feeds on benthic organisms. The high infection rate by this larval parasite may hint to the important role of this species as intermediate host. In case of the species D. (C.) romani the life cycle is still unknown and further studies are needed to identify the intermediate hosts. The monogenean Tinrovia mamaevi was recorded in the upper slope mainly during the spring season. Usually, several studies observed monogeneans in ‘shallower’ waters of the deep ocean only (up to 1,000 m) (De Buron & Morand 2004) and the overall diversity is considered to be lower compared to shallow coastal waters (Rohde 1988). In this study, the higher prevalence at the upper slope could be related to higher host densities observed in these depths, but also to temperature and salinity. Though, the measured variations for these parameters between depth strata were marginal therefore, we argue that additionally other abiotic parameters may influence its spatial and temporal distribution. Finally, the samples obtained for this study contribute to the description of two parasite species new to science, and substantially enhance the knowledge on the parasite fauna of N. bonaparte.

    Metazoan parasite communities and diet of the velvet belly lanternshark Etmopterus spinax (Squaliformes: Etmopteridae): a comparison of two deep-sea ecosystems off northern Spain The first data on metazoan parasite communities and diet composition in Etmopterus spinax at the Galicia Bank and the Avilés Canyon (northwestern Spain, southern Bay of Biscay) are provided in this study. Both areas are topographic underwater features which were included recently in the ‘Natura 2000’ network (Fig. 8.1). This comparative approach focussed on the variation at the level of individual fish hypothesizing that both, parasites and diet, would be informative at detecting differences between the populations of E. spinax in these deep-sea ecosystems. The aim of this study was to combine the examination of stomach contents with the structure of parasite communities, yielding a snapshot of the most recent trophic niche utilisation and reflecting a long-term feeding niche to get more comprehensive information on the role of this shark species in the two local food webs. Parasite communities and diet of 59 specimens of the velvet belly lantern shark, E. spinax, sampled in two underwater features in the Northeast Atlantic off northwestern (Galicia Bank, GB) and northern (Avilés Canyon, AC) Spain have been analysed. Samples of this shark species were taken in summer months of 2010, at 558 (GB) and 855 m (AC) depth. Parasite infracommunity parameters (richness, total abundance, diversity and dominance, parasite abundance) and the number of detected prey items were tested for potential differences between both localities, including host size as covariate. Data on parasite and prey abundance were tested for a potential relationship with host size. The effect of the factor locality and the covariate host size on the composition and structure of the parasite community and diet assemblages were assessed. This was followed by the identification of key taxa mostly contributing to similarities within and dissimilarities between both sampled localities. As far as is known, this study provides the first comparative parasite infracommunity data for a deep-sea shark species. The overall prevalence of infection in E. spinax was 76.3%; overall prevalences and abundances in both areas were not significantly different (overall prevalence: GB: 86.7% vs AC: 65.5%; total mean abundance GB: 5.30 vs AC: 9.52). Overall eleven parasite taxa were recovered from both areas, and the majority of taxa was represented by larval stages (84.4%) (Table 8.1). Three species are recorded for the first time in E. spinax: the cestodes Ditrachybothridium cf. macrocephalum Rees, 1959 (Diphyllidea) and Sphyriocephalus sp. (Trypanorhyncha), and the digenean Otodistomumcf. cestoides (van Beneden, 1871) (Hemiuroidea). Fishes from the GB were significantly larger than in the AC and size could be associated with the abundance of four taxa in the GB and two in the AC, where most correlation were positive except for the monogenean Squalonchocotyle spinaci, which revealed a negative association with host size.

    We detected nine taxa (6 larval and 3 adult stages) at the GB and seven taxa (5 larval and 2 adult stages) at the AC, while five taxa (3 larval and 2 adult stages) occurred in both localities. The component parasite communities in E. spinax were relatively rich for both areas, whereas the infracommunities were rather depauperate, with similar low diversity at both localities (Table 8.2). The differentiation of parasite community composition and structure could be associated with locality (Fig. 8.2), but also indicated that these parameters are affected by host size. The key discriminating taxa contributing to the high dissimilarity (82%) between both localities (GB and AC) were Anisakis sp. (Type I sensu Berland, 1961), larval tetraphyllideans and the monogenean Squalonchocotyle spinaci. While Anisakis sp. was significantly more abundant in samples from the AC, S. spinaci was detected in samples from the GB only. Of the 59 specimens examined 40.7% had empty stomachs. In both areas main prey items consisted of crustaceans, mainly carideans and euphausiids, and fishes, whereas squid and echinoderms were of minor importance (Table 8.3). While sharks from the GB mostly preyed on carideans and bathypelagic fishes, at the AC euphausiids and carideans had the highest contribution to the diet, followed by bathy- and benthopelagic fishes. At the GB host size could not be associated with prey abundance while abundances of euphausiaceans in the AC showed significant negative correlations with host size. The composition and relative abundance of prey was partly explained by locality and host size, where euphausiaceans, carideans and fishes were the key discriminating prey items contributing to the dissimilarity (92.5%) between sampling localities. The total abundance of euphausiids was significantly different between both localities, as it was absent in GB. The significant differences in the composition and structure of both parasite communities and prey assemblages indicate differential effects of the two deep-sea ecosystems (GB and AC) on both long-term and most recent trophic niches of E. spinax. The here observed relatively high richness of component communities, and the depauperate infracommunities in E. spinax, which are strongly dominated by a single species (Table 8.1), may represent a characteristic feature of small sharks. Host size played a certain role with respect to the detected differences in parasites and diet between both localities. Larval cestodes and nematodes were accumulated during host growth with high abundances in larger sharks. This study revealed clear variations in the diet on a very small spatial scale. Euphausiids were of higher importance for smaller shark specimens in the AC, while in the GB these crustaceans exhibited a lower abundance. This also indicates to the already observed opportunistic feeding habits of E. spinax (e.g. Dimech et al. 2012), feeding on most abundant prey items. But it also indicates that larger specimens alter their diet, which was already observed in previous studies, in order to meet higher energetic requirements. The higher abundance of the nematode Anisakis sp. in the AC might be explained by the higher numbers of its definitive hosts detected in the southern Bay of Biscay (López et al. 2004), especially piscivorous and teuthivorous toothed whales (López pers. com.), and probably, to the high amount of discards (fish and viscera) due to enhanced fishing effort in that area (Punzón et al 2010). This may facilitate the infection of all host types by this nematode. The detection of concordant differences in the abundances of euphausiids and Anisakis sp. in the Aviles Canyon linked both most recent and long-term trophic niches. Free-living larvae of monogeneans such as S. spinaci depend on several abiotic factors (Grutter 1998) and the physical-chemical conditions of the GB seabed could be more suitable for this monogenean. Additionally potential schooling behaviour, especially of younger sharks, may promote parasite transmission (Raeymaekers et al. 2008, Jacoby et al. 2011). The presented results underline the importance of the use of multivariate analyses for the assessment of geographical variation in shark populations based on parasites and diet data. This study could serve as a starting point for future studies focussing on potential migration and population connectivity of E. spinax within this geographical area and between the GB and AC. This would also help to define the importance of these protected deep-sea areas (Natura 2000 network) for small sized deep-sea shark populations.

    First insight into the diet and parasite communities of the deep-sea shark Deania profundorum (Smith & Radcliffe, 1912) from the Avilés Canyon (southern Bay of Biscay): shedding light on host’s role? Owing to the partly high importance of elasmobranchs in the deepwater communities in areas of the southern Bay of Biscay (Sánchez et al. 2008), this study shall provide an insight into the role of the centrophorid Deania profundorum within the community of the Avilés Canyon (AC) combining the description of the recent trophic niche (stomach contents) and the long-term feeding niche utilization (parasite communities). We present information on the parasite communities and diet of the arrowhead dogfish, D. profundorum, sampled in an underwater canyon system in the Northeast Atlantic off northern Spain. The samples of this shark species were taken in the Avilés Canyon (AC) (Fig. 9.1), which is part of the ‘Natura 2000’ network, in June 2010 and May 2011 at 580 and 1,260 m depth. The host size was tested for a potential relation to parasite abundances and prey item number. The potential effect imposed by the factors, years and host sex, on several infracommunity parameters (abundance, richness, diversity, dominance, parasite abundance ) and diet were tested including host size as covariate. Community similarity analyses and multivariate analyses were performed to assess the potential effects of sampling years and host sex, including host size as covariate, on the composition and structure of parasite communities and diet assemblages. This is the first comprehensive study on the parasite community and diet of this species in the Northeast Atlantic. We examined 29 specimens of D. profundorum which exhibited an overall prevalence of 89.7% and a total mean abundance of 42.2±71.6. Nine parasite species were detected, of these five were found as larval stage comprising the majority of all identified parasite individuals (88.7%) (Table 9.1). Six out of nine taxa are recorded for the first time in D. profundorum and one species (Squalotrema sp.) could be a species new to science.

    Both sampling years did not differ in sex ratio, host size, or parasite infracommunity parameters, therefore the comparison between sexes were performed with pooled data of both years. Host size was associated with infracommunity parameters (abundance, richness, diversity) and with abundances of three taxa (Deanicola sp., Lacistorhynchidae gen. sp. and Anisakis sp. (Type I sensu Berland, 1961)) showing a positive correlation (Fig. 9.2). The sex ratio was balanced, and males were only slightly larger. Infracommunity parameters did not reveal significant differences between sexes (Table 9.2). Host sex was also not affecting the community similarity, where host size explained a part of the variations observed. However, GLMs analyses indicate that two parasite species, larval Anisakis sp. (Type I sensu Berland, 1961) and lacistorhynchid larvae were significantly more abundant in males (Fig. 9.3). Of the 29 examined specimens 37.9% had empty stomachs. The diet of D. profundorum consisted of fishes, crustaceans (carideans) and squid – with bentho- and bathypelagic fishes as most abundant prey (Table 9.3). None of the prey items could be related to host size and factors years and host sex did not show any effect on the composition of the diet assemblage. The high representation of larval stages of cestodes and nematodes indicates that this shark has an intermediate position in the local food-web, which is also supported by the composition of its diet mentioned above. Host size clearly influenced the parasite community with increasing load observed for larger shark specimens indicating an accumulation during growth. This pattern was already observed in other studies, where parasite abundance and richness increased with host size (e.g. Timi & Poulin 2003, Bagge et al. 2004), as parasites are acquired and accumulated over the life span (Barber & Poulin 2002). The comparison with conspecific, congeneric and other shark species partly indicated the same pattern of increasing parasite load, while the observed different parasite diversity and richness indicate, amongst other parameters, to distinct species related feeding habits (e.g. Dallarés 2016). The host size also explains the differences observed for single parasite species between sexes, where slightly larger males exhibited higher abundances of larval Anisakis sp. and lacistorhynchid larvae. These differences between sexes may indicate to potentially distinct feeding habits of both sexes which could not be discerned by the diet analysis. This study highlights the previous suggestions on the importance of using parasites as biological indicators to identify potential prey items of past feeding events, and the assessment of the host role in marine communities. Further, this survey on the diet and metazoan parasite communities of this shark provides the first data from this area and adds some new data to the scant information available for this genus. Future studies could clarify the potential role of underwater features (canyons, seamounts) on the diet and parasite community of benthopelagic shark species, especially when comparing these parameters from areas without these topographic features.