Marys Medicine

Marine ecology progress series 530:119

Guerreiro et al.: Isotope values of Southern Ocean cephalopods Fig. 7. Individual principal component scores (from PC1 and PC2 displayed in Fig. 6) of each sample area (SG = South Georgia, CRZ = Crozet Islands, KRG = Kerguelen Islands) and squid species: = Alluroteuthis antarcticus, = teuthis skolops, = Histioteuthis eltaninae, = glacialis, = Gonatus antarcticus, = Histioteuthis atlan tica Histioteuthis atlantica (small), = ingens, = Moroteuthis knipovitchi, = Konda kovia longi- Martialia hyadesi, = ?Mastigoteuthis sp. A Taonius sp. (Clarke), = Taonius sp. B (Voss), = Cycloteuthis akimushkini, = Taningia danae, = Fig. 8. Dendrograms produced by Cluster Analysis (using standardized variables and Ward's linkage method) showing aggre-gations of species and sample areas (SG = South Georgia, CRZ = Crozet Islands, KERG = Kerguelen) based on δ15N (upperpanel) and δ13C (lower panel) data, and their functional classification (below each dendrogram). ALLU = Alluroteuthis antarcti-cus, BATO = Batoteuthis skolops, CYCLO = Cycloteuthis akimushkini, ELTAN = Histioteuthis eltaninae, GALIT = Galiteuthisglacialis, GONAT = Gonatus antarcticus, HALIPH = Haliphron atlanticus, HatlantL = Histioteuthis atlantica (large), HatlantS =Histioteuthis atlantica (small), INGENS = Moroteuthis ingens, KNIPO = Moroteuthis knipovitchi, KONDA = Kondakovia longi-mana, MART = Martialia hyadesi, MAST = ?Mastigoteuthis sp. A (Clarke), TANING = Taningia danae, TAON = Taonius sp. (Clarke), TAON B = Taonius sp. B (Voss) Mar Ecol Prog Ser 530: 119–134, 2015 guelen (south vs. north of the APF, respectively).
Also, some squid from higher latitudes (e.g. Moro- teuthis knipovitchi, Table 4) in Kerguelen showed lower δ13C values than the same species from the lower latitude site at Crozet. However, this was not true in all species (e.g. M. hyadesi and Histioteuthis atlantica, Table 4), possibly due to the higher base-line δ13C of the Kerguelen Plateau (Trull et al. 2008).
To enable comparison with other studies, the mean isotope ratio in soft tissue was estimated, by subtract- ing 0.75 ‰ from the δ13C values measured in the beaks (Hobson & Cherel 2006). These corrected val- n Ocean and infer ues and their assigned distribution (Cherel & Hobson ; ?: no known distribution for this species 2007, Jaeger et al. 2010) was then contrasted with previous assessments (Xavier et al. 1999, Collins & Known distribution Rodhouse 2006, Xavier & Cherel 2009) (Table 4).
Cephalopod species that were previously considered to live at high latitudes (according to Xavier et al.
1999, our Table 4) — Batoteuthis skolops, Kondakovia osses in the Souther longimana and M. knipovitchi — had the lowest mean δ13C (and high standard deviations, except for B.
skolops). Surprisingly, G. antarcticus also displayed very low values, despite previous evidence that it ismostly distributed in northern sub-Antarctic waters ssessed water mass (Xavier et al. 1999, Collins & Rodhouse 2006). The high standard deviation in δ13C recorded in K. longi- mana and M. knipovitchi, and low mean values in opical waters (see Fig. 1); Cos.: cosmopolitan G. antarcticus can be explained by a broader distri -bution of these species, including north and south of the APF, in agreement with Cherel & Weimerskirch (1999). Therefore, these 3 species (K. longimana, M. knipovitchi and G. antarcticus) are distributed across the APF (both in Antarctic and sub-Antarctic waters), whereas B. skolops is found exclusively in Antarctic waters (Fig. 5, Table 4). The so-called subtropical spe- cies that were sampled (Taonius sp. [Clarke], Taonius sp. B [Voss 1980], Cycloteuthis akimushkini and His-tioteuthis atlantica [Voss et al. 1998]) (Table 4), were those with the highest δ13C, indicating distributions that are around and to the north of the STF (Fig. 5, ctic; Sub-Ant.: sub-Antar δ13C values typical of sub-Antarctic waters were ob- tained for numerous species (Haliphron atlanticus, on atlanticus Taningia danae, M. ingens, M. hyadesi, H. eltani- oteuthis antar nae, Taonius sp. B [Voss], Alluroteuthis antarcticus, tialia hyadesi oteuthis ingens C in the mantle (muscle) of the main squid species in the diet of wandering albatr aningia danae Galiteuthis glacialis and ?Mastigoteuthis sp. A Gonatus antar [Clarke]) (Fig. 5, Table 4). Collins & Rodhouse (2006)and Xavier et al. (1999) considered that A. antarcticusand G. glacialis live primarily in Antarctic waters; however, our isotopic data suggest that some indi viduals inhabit sub-Antarctic waters (Table 4).
Furthermore, clustering of species based on es-ence, 0 = absence. Ant.: Antar able 4. Estimated (Fig. 8), supports the biogeographic assessment dis- Guerreiro et al.: Isotope values of Southern Ocean cephalopods cussed above. The 3 clusters distinguished in that skolops, G. antarcticus, Taonius sp. B (Voss) and analysis correspond unequivocally to cephalopods Taningia danae; and finally (3) the subtropical squid originating from Antarctic, sub-Antarctic or (near to) C. akimushkini, Histioteuthis atlantica and Taonius subtropical waters.
sp. (Clarke). This classifi cation is confirmed by themultivariate analysis (Figs. 7 & 8), which distin-guished 2 large, well-defined groups (with M. hya - Beak δ15N values and trophic relationships
desi and group (1) in the first, and groups (2) and (3)in the second) (Fig. 8).
Several cephalopod species showed higher δ15N By correcting the measured δ15N values for beaks in samples from South Georgia than from the other to provide estimates for soft tissue (by adding 4.86 ‰; island groups (especially Crozet), which suggests Hobson & Cherel 2006), and comparing these re sults that either squid at South Georgia have different with muscle samples collected in previous studies in feeding preferences (higher trophic level) from those the same regions (Tables 5 & 6), it is possible to infer in the Indian Sector, or there are regional differences potential prey. However, this is with the caveat that in primary productivity that lead to differences in these correction factors may not be appropriate for all δ15N baselines between regions, relating to the rela- species. Nevertheless, the most probable niches occu- tive dominance of eukaryote vs. prokaryote (auto- pied by these animals are as follows. M. hyadesi is trophic) production (Fawcett et al. 2011). Regardless, known to feed mainly on hyperiid am the present study largely confirms previous findings myctophid fish, and to a lesser extent on cephalo based on stable isotope analysis for most of the stud- pods, including a degree of cannibalism (Rodhouse ied species (Cherel & Hobson 2005, Cherel et al.
et al. 1992). Since myctophid fish tend to be at a sim- 2008), with the exception of K. longimana and G. ilar or higher trophic level based on nitrogen isotope antarcticus, for which δ15N values were higher than ratios (Tables 5 & 6) (Cherel et al. 2008), it seems that those recorded previously (Wada et al. 1987, Cherel M. hyadesi feeds on myctophids in lower quantities & Hobson 2005, Cherel et al. 2008).
than previously suggested, at least in the southern The distribution of δ15N in the different species Indian Ocean. K. longimana presented very low δ15N suggested 3 distinct groups and one outlier (M. values (and high LRL; Fig. 7), but not low enough hyadesi). The 3 groups were: (1) the onychoteuthid to be entirely dependent on euphausiids (Table 5) squids (with the lowest δ15N values, especially K. (Nemoto et al. 1985, 1988), and thus its diet seems longimana) plus Haliphron atlanticus, H. eltaninae, likely to include some prey with low δ15N values such cialis; (2) ?Mastigoteuthis sp. A (Clarke), B. as crustaceans and myctophid fish (Table 6) (Kaehler Table 5. Estimated δ15N values in mantle (muscle) of the main squid species in the diet of wandering albatrosses at South Georgia, Crozet Kerguelen Islands Taonius sp. (Clarke) Taonius sp. B (Voss) Histioteuthis atlantica small 10 15.2 ± 1 13.7−16.9 Histioteuthis atlantica Large ?Mastigoteuthis sp. A (Clarke) 10 13.6 ± 1 12.3−15.1 Martialia hyadesi Taningia danae Mar Ecol Prog Ser 530: 119–134, 2015 Table 6. Trophic level and δ15N of squid, crustacea and marine vertebrates sampled in previous studies in the Southern Ocean Cherel et al. (2008) Stowasser et al. (2012) Cherel et al. (2008) Prince Edward Is.
Kaehler et al. (2000) Euphausia superba Cherel et al. (2008) Stowasser et al. (2012) Stowasser et al. (2012) Euphausia frigida Stowasser et al. (2012) Stowasser et al. (2012) Cherel et al. (2008) Cherel et al. (2008) Stowasser et al. (2012) Cherel et al. (2008) Stowasser et al. (2012) Cherel et al. (2008) Stowasser et al. (2012) Cherel et al. (2008) Stowasser et al. (2012) Cherel et al. (2008) Cherel & Hobson (2005) Cherel et al. (2008) Cherel & Hobson (2005) Martialia hyadesi Cherel et al. (2008) Cherel & Hobson (2005) Cherel et al. (2008) Cherel & Hobson (2005) Cherel et al. (2008) Cherel & Hobson (2005) Cherel et al. (2008) Cherel & Hobson (2005) Stowasser et al. (2012) Pauly et al. (1998) Burns et al. (1998) Zhao et al. (2004) Hydrurga leptonyx Hall-Aspland et al. (2005) Zhao et al. (2004) Anderson et al. (2010) Stowasser et al. (2012) Diomedea exulans Anderson et al. (2010) Jaeger et al. (2010) Anderson et al. (2010) Cherel et al. (2013) Anderson et al. (2010) Cherel et al. (2007) Cherel et al. (2008) Cherel et al. (2007) Stowasser et al. (2012) aAdélie Land; bCorrected (beak) values; cRaw (beak) values Guerreiro et al.: Isotope values of Southern Ocean cephalopods et al. 2000, Cherel et al. 2008, Stowasser et al. 2012).
subtropical waters (Altabet & François 1994, Jaeger M. ingens (and M. knipo vitchi) had a similar niche to et al. 2010). C. akimushkini had the highest mean K. longimana (Table 5), which was also within the δ15N value of all species, and there was a positive expected range for a diet dominated by mesopelagic relationship between individual size and δ15N in H. fish (myctophids and paralepids, Table 6) (Cherel & atlantica (Table 1, Fig. 7). This squid feeds higher in Duhamel 2003).
the food chain as it grows and is able to feed on pro- The cephalopods which had the lowest δ15N (apart gressively larger prey. Thus, ontogenetic variation from M. hyadesi and the onychoteuthids, Table 5) has a potentially marked impact on δ15N values in are likely to depend on zooplankton that feed in turn histioteuthids as it does in other species of ommas- on sinking organic matter, since the measured δ15N trephids and onychoteuthids (Cherel & Hobson 2005, values were higher than expected from organisms Cherel et al. 2009a, Lorrain et al. 2011).
that, in some cases, are characterized by gelatinous Even though the various squid species in this study bodies and small size (except for Haliphron atlanticus, showed significant intra-specific differences in their Fig. 7), e.g. cranchiids (Collins & Rodhouse 2006).
niches across island groups, they generally remained The sinking organic matter and detritus is generally in the same relative positions within the respective enriched in 15N as a consequence of microbial cephalopod communities. The exception was ?Masti - decomposition during the transport to depth, which goteuthis sp. A (Clarke) which moved between the richment in the whole food web first group in Crozet to the second group in South (including cephalo pods) that is dependent on this Georgia (Figs. 2, 3, 4 & 8).
resource (Michener & Kaufman 2007).
Overall, the squid that live in Antarctic and sub- G. antarcticus presented the highest δ15N of all Antarctic waters were secondary to tertiary con- cephalopods in this study (apart from T. danae and sumers, i.e. trophic level (TL) > 3, which is near the the subtropical squids, Table 5). These high δ15N average level for marine mammals (TL = ca. 4.0 values are just below those for the colossal squid [Pauly et al. 1998]), penguins (TL = 3.4−4.0 [Sto Mesonychoteuthis hamiltoni (Cherel & Hobson 2005, wasser et al. 2012]) other seabirds (TL = 3.7−5.2 [Sto - Cherel et al. 2008) (Table 6), which is considered a wasser et al. 2012]), and sharks (TL > 4 [Cortés 1999]) top invertebrate predator (Cherel & Hobson 2005) (Table 6). Furthermore, the range of isotopic niches that feeds on large fish and squid, and is found in the occupied by squid, and their wide horizontal and diet of sperm whales Physeter macrocephalus and vertical distribution, shows parallels with the niches sleeper sharks Somniosus cf. microcephalus (Clarke occupied by large pelagic fish (Rodhouse & White 1980, Cherel et al. 2004) (Table 6). This may probably 1995, Cortés 1999). Indeed, at depth, squid may be be explained by a top predator position (by G. competing for prey with large, deep-diving mammals antarcticus) on a rather inefficient food web charac- such as seals (Cherel et al. 2008). The most likely terized by high 15N enrichment rates, dependent on candidates for occupying the niche of large pelagic heterotrophy of organic matter and detritus descend- fish are the squids with the highest δ15N that do not ing from epipelagic waters. As they are muscular belong to the cranchiid or the mastigoteuthid/bato- squid with well-developed hooks, which is a sign of teuthid families, as the former are gelatinous and an active predator among squid, this species is a can- likely to be sluggish (Collins & Rodhouse 2006) and didate for top predator within this environment (ac - the latter probably depend on the benthos (Roper & cording to the isotope data), despite their small size Vecchione 1997); hence, the most active predators relative to such megafauna as T. danae (Fig. 7) and M. are presumably G. antarcticus, T. danae and M. knipovitchi (Figs. 2–5).
T. danae is certainly one of the top predators amongst the squid inhabiting the deep ocean (Cherelet al. 2009b), as it shows a nitrogen isotope ratio at least as high as the giant squid Architeuthis dux, andwithin the range recorded in other studies (Cherel In conclusion, our study emphasizes that cephalo - & Hobson 2005, Cherel et al. 2009b) (Tables 5 & 6). T. pods have a wider and generally more complex (but danae can also reach a considerable size (Fig. 7), well defined) pattern of distribution around the with a maximum mantle length of 170 cm (Nesis Southern Ocean than previously considered. Given 1987). The subtropical species Histioteuthis atlantica, the large range of δ13C and δ15N values, cephalopods mush kini and Taonius sp. (Clarke) had the must occupy a diverse range of niches, from the mid- highest δ15N, probably due to the high baseline in dle of the food web (secondary consumers, TL = 3), to Mar Ecol Prog Ser 530: 119–134, 2015 top predators (TL > 4) in all the different water masses of the Southern Ocean. δ15N in our samples ingens (Teuthoidea: Onychoteuthidae) in the upperslope waters of the Kerguelen Islands. Mar Ecol Prog Ser corresponded broadly to those expected from previ- ous conventional diet studies, or, with the exception of Martialia hyadesi, were somewhat higher, sug- predators: a new tool to study the trophic ecology of gesting a greater representation of higher trophic cephalopods, including giant and colossal squids. Proc RSoc B 272: 1601−1607 prey. Although particular squid varied in their iso- topic niche depending on the sampling site (island bon stable isotope signatures of marine predators: a tool group), they did, however, occupy the same relative to investigate their foraging areas in the Southern position within each community, apparently consist- Ocean. Mar Ecol Prog Ser 329: 281−287 ing of 3 main groups and one outlier (M. hyadesi).
Cherel Y, Klages N (1998) A review of the food of alba- trosses. In: Robertson G, Gales R (eds) Albatross biology The most active, muscular and best-armed (hooked) and conservation. Surrey Beatty and Sons, Chipping cephalopod species with the highest δ15N levels seem Norton, Australia, p 113–136 likely to occupy the niche of a top predator in pelagic ecosystems. Squid in general constitute a crucial and marine resources: black-browed albatrosses feeding onommastrephid squids in Kerguelen waters. Mar Ecol diverse component of Southern Ocean ecosystems, Prog Ser 129: 295−300 as not only are they widespread and abundant prey for marine top predators, but in addition, the meso- teuthid squids in the southern Indian Ocean: new infor- and bathypelagic species function as effective bio- mation from seabird predators. Mar Ecol Prog Ser 188: 93−104 logical circulators by returning deep-sea carbon back to the surface, and vice-versa. Finally, our study subantarctic islands: new information from predators.
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