New records of early life-stages of cephalopods in the Chiloe Interior Sea/Nuevos registros de estadios de vida tempranos de cefalopodos en el mar interior de Chiloe.
Several studies have shown that early life stages of many cephalopods species are closely associated with oceanic current systems, where eggs masses, paralarvae and even juveniles, can actively be transported from spawning areas to their feeding grounds (reviewed by Rocha et al., 1999). Although such studies are of major relevance, the distribution and role of early life-history stages of cephalopods in marine trophodynamics (i.e. as predators or prey) is not yet fully understood (Boyle & Rodhouse, 2005; Jackson et al., 2008).
For most of the ~80 cephalopod species recorded in Chilean waters (Rocha, 1997; Ibanez et al., 2009; Vega 2009), young forms are still not known, and field studies on taxonomy, abundance and distribution of paralarval or juvenile stages remain limited (Vega et al., 1999, 2000) (Table 1). The current study provides additional information about taxonomic identification, size structure, abundance and geographic distribution of early life stages of cephalopods collected in a small section of the Chilean fjord region (41[degrees]-43[degrees]S).
Young stages of cephalopods were collected aboard the vessel AGOR "Vidal Gormaz" during CIMAR 11 Fiordos cruise (November 2005). Sampling was conducted at 19 oceanographic stations between Seno de Reloncavi (41[degrees]31'S) and Boca del Guafo (43[degrees]39'S), southern Chile (Fig. 1a). Oblique hauls were performed from 200 m depth to the surface using a Bongo net (350 um mesh; 60 cm diameter) or a Tucker trawl (300 um mesh; 1 [m.sup.2] diameter) equipped with a flowmeter to estimate the volume of sea-water filtered, ranging from 140 [m.sup.3] (range: 101 to 179 [m.sup.3]) in stations where paralarvae were collected, to 98 [m.sup.3] (range: 57 to 188 [m.sup.3]) in stations where paralarvae were not found. Samples were preserved in 5% formalin in sea water solution until further examination. Each individual was identified to the lowest taxonomic level by comparison with descriptions available in the literature (Sweeney et al., 1992; Ortiz et al., 2006; Bolstad 2008; Gonzalez et al., 2008; Ortiz & Re, 2010; Uriarte et al., 2010) using standardized morphological characters, including dorsal mantle length (DML, mm), number and distribution of suckers (S), tentacular club (TC) and chromatophore patterns. Abundance of paralarvae was expressed as ind 1000 [m.sup.-3] and their spatial distribution were plotted in a map of the area provided by the Chilean Army. When possible, samples were compared with adult specimens stored at Museo Nacional de Historia Natural, Chile and reported as MNHNCL with their corresponding storage number.
A total of fifty two specimens were collected, from the families Octopodidae D'Orbigny, 1840; Sepiolidae Leach, 1817 and Onychoteuthidae Gray, 1849 (Table 2). The highest abundances and spatial distributions were observed in oceanic stations (e.g. 38, 47, 49, 50) around Boca del Guafo and Corcovado Gulf, with more than 18 ind 1000 [m.sup.-3] (Figs. 1b-1d). Octo-pods identified as Robsonella fontaniana (D'Orbigny, 1834) were the most abundant, with 46 paralarvae ranging from 2.3 to 4.6 mm DML (Table 2, Fig. 1b). These individuals displayed a muscular body, covered by an unpigmented layer (especially smaller sizes) surrounding the funnel, mantle, eyes and arms. The eyes were large, and the mantle was short and rounded (Figs. 2a-2b). Arrangements of brown chromatophores covered the dorsal and ventral surfaces of the head, mantle, arms (~4) and dorsal surface of the perivisceral epithelium (> 18). Arms were shorter than the mantle. All paralarvae presented an uniserial line of four suckers of similar size (Figs. 2c-2d) and larger individuals also presented, in addition to the uniserial line of four, a variable number of small biserial suckers in development (ranging from 2 to 10) depending on the size of the paralarvae.
Four larger octopods were collected (5.0-12.1 mm DML, Table 2, Fig. 1b), and identified as Enteroctopus megalocyathus (Gould, 1852). An unpigmented layer also surrounded their bodies, only interrupted by the funnel orifice, mantle aperture, and sucker openings. Eyes were large and prominent. The mantle was muscular, broad and rounded (Figs. 2e-2f, 2f). Bodies were dorsally and ventrally spotted with brown chromatophores; however, less numbers were observed in the ventral surface. Arms had a slightly smaller size compared with the mantle, showing 18-36 biserial suckers (depending of DML) arranged in a zig-zag row that gently decreased in size from the mouth towards the tip (Figs. 2g-2h).
Only one paralarva of Sepiolidae was collected (5.5 mm DML), and identified as Semirossia patagonica (Smith, 1881). The mantle was short and broad. Fins were large and separated. Dorsal and ventral surfaces of the body were covered by round and brown chromatophores, except for the edge of the fins (Figs. 2i-2j). Arms were shorter than the mantle, with small biserial suckers markedly enlarged at the medial and distal portion of the series on arms. The TC showed small and numerous suckers that gently decreased in size towards the tips (Figs. 2k-2l).
One 19 mm-DML squid was identified as Onychoteuthidae, but its taxonomic status could not be identified to the species level. The specimen had a muscular body, with a relatively broad mantle pointing out posteriorly. Eyes were large and prominent (Fig. 2m). Dark chromatophores covered the head and dorsal surface of the mantle. The gladius was visible beneath the skin in the dorsal midline (Fig. 2n). Rhombic fins in the posterior end were bisected by the gladius (Fig. 2o). Arms were shorter than the mantle, with stalked suckers (~50-60) decreasing in size from the mouth towards the tip (see schemes: Figs. 2p-2q). Tentacles were slightly longer than arms. TC showed a single row of 9 hooks in the manus, surrounded by ~40 stalked circular suckers with a central aperture. The carpal pad displayed 10 suckers (Fig. 2r).
[FIGURE 1 OMITTED]
The early life stages of cephalopods collected during this survey belong to species that are common in Chilean waters; however, with the exception of some octopuses (e.g. O. mimus, R. fontaniana, E. megalocyathus) and squids (e.g. D. gigas, L. gahi) (Warnke, 1999; Guerra et al., 2001; Castro et al., 2002; Ortiz et al., 2006; Gonzalez et al., 2008; Staaf et al., 2008; Ortiz & Re 2010; Uriarte et al., 2010), detailed information on morphological patterns of hatchlings and juveniles has not previously been described. Although the abundance of young cephalopods in our samples seems to be low, similar values have been previously recorded in this geographic area by Vega et al. (2000) and Balbontin et al. (2004). Causes of these low captures could be their patchy distribution, low densities, or their potential ability to avoid the plankton nets (Sweeney et al., 1992). The comparatively large captures of octopods recorded in this survey at oceanic stations could reflect either the active movements of these visual predators in searching for food, or alternatively, an accumulation of paralarvae due to currents between inshore and offshore waters. In fact, currents play a major role in the dynamic of this complex hydrographic system, attaining values of 66.5 cm [s.sup.-1] in areas close to the sampling site (i.e. Canal Moraleda, Balbontin et al., 2009). The presence of cephalopod paralarvae in previous surveys conducted in this region suggest that Chilean fjords and channels could be important for hatching and breeding not only for benthic octopuses, but also for other species of cephalopods inhabiting this particular area.
[FIGURE 2 OMITTED]
The morphological characters suggested by Sweeney et al. (1992) for species recognition were useful for identifying the young stages collected. Comparisons among laboratory reared paralarvae of the three most common coastal octopuses from Chilean waters: O. mimus, R. fontaniana and E. megalocyathus [DML (1.69 vs 3.18 vs 8.38), number of suckers (3 vs 4-5 vs 16-27), number of visceral chromatophores (6-8 vs 19-33 vs 100-210)] (Warnke, 1999; Castro et al., 2002; Ortiz et al., 2006; Gonzalez et al., 2008; Ortiz & Re, 2010; Uriarte et al., 2010), in addition with the geographic distribution of adult specimens, allowed us to determine the taxonomic identification of the paralarvae collected. From the three above named species, O. mimus is the only one that does not occur in southern Chile (Vega et al., 2001; Ibanez et al., 2009; Vega, 2009). From the other two, E. megalocyathus is the only large octopod (~1 m total length [TL]) recorded in this area (Osorio et al., 2006; Haussermann & Forsterra, 2009), with paralarvae around 8 mm DML and a planktonicbenthic period of dispersal (Ortiz et al., 2006), which could explain the large size of the paralarvae collected. By contrast, for R. fontaniana smaller adult sizes (28 cm TL), smaller hatchling sizes (~4.0 mm TL), extended planktonic periods (~72 days) and large benthic stage size (~11 mm TL) have been recorded (Gonzalez et al., 2008; Ortiz & Re, 2010; Uriarte et al., 2010), supporting the identity of the small paralarvae collected. A skin film covering the body of the paralarvae has been reported in several species of octopuses, including E. megalocyathus (see Villanueva & Norman, 2008); however, it was not detected by Ortiz & Re (2010) in R. fontaniana hatchlings. The presence of this loose skin in the samples of R. fontaniana collected could be an artefact of the fixative process, and should be re-evaluated in live field-collected individuals. Although the function of this skin film is unknown, it is possible that such layer is used to attain neutral buoyancy, potentially aiding passive dispersion (Villanueva & Norman, 2008).
In relation to Sepiolidae, two species have been recorded in southern Chile, Rossia glaucopis and Semirossia patagonica (Ibanez et al., 2009; Vega, 2009); however, only adults of the latter are know from the study area (Valdovinos et al., 2005; Osorio et al., 2006; Hausermann & Forsterra, 2009). For S. patagonica there is no previously published information about embryonic development or paralarval stages in Chilean waters. Sweeney et al. (1992) described for Sepiolidae, subfamily Rossiinae, a size of 5-7 mm in eggs, similar to the size of the young stage collected in this survey. S. patagonica might be confused with R. galucopis; however, only the former possess enlarged suckers in the arms, a clearly visible trait in both the paralarva collected and in one adult specimen stored at Museo Nacional de Historia Natural, Chile (MNHNCL, No. 1979).
For Onychoteuthidae, records from the southeastern Pacific coast (i.e. 42[degrees]S-56[degrees]S) describe the occurrence of five species in Chilean waters (i.e. Onychoteuthis banksii, Kondakovia longimana, Moroteuthis ingens, M. knipovitchi and M. robsoni) (Rocha, 1997; Vega et al., 2001; Ibanez et al., 2009; Vega, 2009). A recent taxonomic revision of the family also suggested the occurrence of Onykia (Moroteuthopsis) ingens between 30[degrees]S and 60[degrees]S, which, however, would be a new combination for Moroteuthis ingens (Bolstad, 2008). Despite difficulties in Onycoteuthid's systematics, the juvenile collected in this survey showed the typical morphological characters used to identify members of this family, such as the gladius visible as a dark line running length of the dorsal mantle with a pointed rostrum bisecting the fins. The TC showed a single row of hooks in the manus (double row in adults); however, because hooks begin to develop around 15 mm (Bolstad, 2008), it is possible that they were just partly developed in this juvenile squid, which probably corresponds to Onykia sp. (K. Bolstad, pers. comm.). Nevertheless, because there is no information available on young onychoteuthis from Chilean waters, detailed studies and sampling are still needed to clarify the specific identity of this individual.
The knowledge of the marine flora and fauna of this fjord region is still in a discovery phase, and has been hampered by difficulties in sampling this relatively isolated area. Results from previous oceanographic surveys (e.g. CIMAR 1, 3, 4, 7, 9, 11, 12) and from recent biodiversity expeditions (Haussermann & Forsterra, 2009) have substantially increased the information available for this region. The efforts made in the present survey have also provided new and valuable information to partially fulfill the current knowledge gap about early life stages of cephalopods from Chilean and southeastern Pacific waters.
Authors thank to the Comite Oceanografico Nacional (CONA), commander, crew and technicians aboard AGOR Vidal Gormaz for samples collection. Dr. Sergio Palma and Laboratorio de Planctologia for samples separation. Dr. Sergio Letelier and Dr. Kat Bolstad provided valuable advices identifying the specimens. Juan Pablo Saez made all the schematic draws. The comments of anonymous reviewers that improved initial versions of the manuscript are also appreciated.
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Received: 6 December 2010; Accepted: 18 December 2011
Sergio A. Carrasco (1), Roberto Maltrain (2), Francisco Villenas (3), Marco A. Vega (4)
(1) School of Biological Sciences and Coastal Ecology Laboratory, Victoria University of Wellington Wellington 6140, New Zealand
(2) Facultad de Ciencias del Mar y de Recursos Naturales, Universidad de Valparaiso Casilla 5080, Vina del Mar, Chile
(3) Escuela de Ciencias del Mar, Pontificia Universidad Catolica de Valparaiso Casilla 1020, Valparaiso, Chile
(4) Departamento de Ciencias Basicas, Universidad Santo Tomas Heroes de la Concepcion 2885, Iquique, Chile
Corresponding author: Sergio Carrasco (email@example.com)
Table 1. Previous records of early life stages of cephalopods collected along the Chilean coast. Tabla 1. Previos registros de estadios tempranos de cefalopodos recolectados a lo largo de la costa de Chile. Date Area Family 1998 Mejillones, northern Chile Gonatidae (23[degrees]S) Bolitaenidae Ommastrepidae Chiroteuthidae Cranchiidae Octopodidae 1998-99 Canal Moraleda, southern Chile Octopodidae (43[degrees]S-46[degrees]S) Gonatidae Date Species Number of MDL range paralarvae (mm) 1998 Gonatus sp. 6 3.9 - 17 Japetela sp. 4 2.9 - 9.8 Ommastrepidae ind. 1 3.9 Ciroteuthis sp. 1 - Teuthowenia sp. 1 - Octopodidae ind. 1 - 1998-99 Octopus sp. 13 2.1 - 8.3 Gonatus antarcticus 1 5 Date Reference 1998 Vega et al. (1999) 1998-99 Vega et al. (2000) (-) Unknown, specimens were not in a good enough condition to estimate DML. Table 2. Early life stages of cephalopods collected in the present study, southern Chile (CIMAR 11 Fiordos cruise, 41[degrees]S-43[degrees]S). Tabla 2. Estadios tempranos de cefalopodos recolectados en el presente estudio, Sur de Chile (Crucero CIMAR 11 Fiordos, 41[grados]S-43[grados]S). Station Depth (m) Gear Date Family 16 0 - 20 Bongo net 8/11/2005 Octopodidae Onychoteuthidae 32 0 - 20 Bongo net 8/11/2005 Octopodidae Sepiolidae 38 0 - 100 Bongo net 19/11/2005 Octopodidae Octopodidae 47 0 - 150 Bongo net 14/11/2005 Octopodidae Octopodidae 49 0 - 200 Bongo net 14/11/2005 Octopodidae 50 0 - 70 Tucker trawl 14/11/2005 Octopodidae 50 0 - 100 Tucker trawl 14/11/2005 Octopodidae Station Species Number of DML range paralarvae (mm) 16 Enteroctopus megalocyathus 1 6.5 Onychoteuthidae indet. 1 19 32 Enteroctopus megalocyathus 1 8.6 Semirossia patagonica 1 5.5 38 Enteroctopus megalocyathus 2 5.3 - 12.1 Robsonella fontaniana 6 2.3 - 3.1 47 Robsonella fontaniana 1 3.6 Enteroctopus megalocyathus 1 5.0 49 Robsonella fontaniana 3 3.2 - 3.9 50 Robsonella fontaniana 13 2.6 - 4.0 50 Robsonella fontaniana 22 2.5 - 4.6