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MORPHOMETRIC CHANGES AND GROWTH
RATE DURING EMBRYONIC DEVELOPMENT OF
ROBSONELLA FONTANIANA
I. Uriarte, O. Zuñiga, A. Olivares, V. Espinoza, V. Cerna, A. Farías, C. Rosas
To cite this version:
I. Uriarte, O. Zuñiga, A. Olivares, V. Espinoza, V. Cerna, et al.. MORPHOMETRIC CHANGES AND GROWTH RATE DURING EMBRYONIC DEVELOPMENT OF ROBSONELLA FONTANIANA. Vie et Milieu / Life & Environment, Observatoire Océanologique - Laboratoire Arago, 2009, pp.315-323. �hal-03253776�
INTRODUCTION
Robsonella fontaniana (D’Orbigny, 1834) is a
small-sized pygmy octopus found off southern Chile and Argen-tina. Some reproductive studies of R. fontaniana have shown that this species can easily spawn up to 2500 eggs (Briceño-Jacques 2004, González et al. 2008). Morpho-metric and graviMorpho-metric changes have also been described for R. fontaniana paralarvae and juveniles up to 160 days after hatching (Uriarte et al. 2009). Another study consid-ered the effects of temperature and feeding on paralarvae (González et al. 2008) and the effect of diet on digestive enzyme modulation during the paralarval phase (Pereda
et al. 2009). Given the advanced knowledge of the
spe-cies’ biological aspects, R. fontaniana could be used as a reference model for rearing other cephalopod species with planktonic phases (Gonzalez et al. 2008, Uriarte et al. 2008, 2009, Pereda et al. 2009).
Several authors have suggested that the transition from yolk utilization to active predation is a critical period in the early life history of cephalopods that depends on the embryonic yolk reserves (e.g. Boyle & Chevis 1992, Han-lon & Wolterding 1989, Naef 1928, Vecchione & Hand 1989, Vidal & Haimovici 1998), similar to the critical period concept described for octopus paralarvae (Villan-ueva & Norman 2008). According to Boletzky (2003), the volume of yolk remaining in the inner sac at hatching is
one of the major factors influencing the initial feeding conditions of the hatchlings. Thus, evaluations of embry-onic yolk reserves could constitute the basis for a quality criterion for hatchlings. Such information could be useful for both aquaculture and fisheries management.
Variations in individual growth influence many facets of a cephalopod population such as its size and age struc-ture, reproductive dynamics, and hatchling survival rate. Ontogenetic changes in size and shape influence an ani-mal’s locomotion as it grows. Villanueva et al. (1996) observed strong morphometric changes in O. vulgaris paralarvae and juveniles that dramatically influenced their swimming capacities and, at the same time, their predato-ry abilities. However, no similar studies indicate how embryonic growth determines the exponential growth curves observed in the first part of the cephalopod life cycle (Mangold 1983). In a previous study, Uriarte et al. (2009) observed drastic morphometric changes in R.
fon-taniana related to the logarithmic growth of the mantle
with respect to the total length, as compared to the organs related directly to catching prey (e.g., arm length and eye diameter), which grow linearly with respect to total length. Herein, we provide morphometric and gravimetric analyses of R. fontaniana embryos in order to determine whether the exponential growth curves observed in the paralarvae during the planktonic phase begin during the embryonic phase of development. Yolk reserves and
pro-MORPHOMETRIC CHANGES AND GROWTH RATE DURING
EMBRYONIC DEVELOPMENT OF ROBSOnella fOntaniana
i. uRiaRte
1,2*, O. ZuÑiGa
3, a. OliVaReS
3, V. eSPinOZa
1,
V. CeRna
1, a. faRÍaS
1,2, C. ROSaS
41 instituto de acuicultura, universidad austral de Chile, PO Box 1327, Puerto montt, Chile 2 Cien austral, Puerto montt, Chile 3 facultad de Recursos del mar, universidad antofagasta, antofagasta, Chile 4 unidad multidisciplinaria de docencia e investigación, facultad de Ciencias,
universidad nacional autónoma de méxico, Sisal, Yucatán, mexico * Corresponding author: iuriarte@spm.uach.cl
ABSTRACT. – During paralarval development of the octopus Robsonella fontaniana, the man-tle size is reduced in proportion to the total octopus length, whereas the organs more directly involved in catching prey tend to increase in direct proportion to the total length. A morphomet-ric and gravimetmorphomet-ric study of R. fontaniana embryos was made in order to determine whether the morphometric trends and exponential growth rates observed in the planktonic and benthic phas-es begin during the embryonic development. Seven clutchphas-es, sampled during different seasons of the year, were studied under controlled conditions until hatching of the planktonic paralarvae. Yolk reserves and protein content in the perivitelline liquid were quantified to determine how the yolk absorption and the consumption of perivitelline protein are modulated during embry-onic development. Results demonstrate that during embryembry-onic development the growth rate for total length, mantle length, and arm length is exponential, indicating that the type of growth described for paralarvae and juveniles begins during embryonic life. The morphometric changes and growth are related to an exponential reduction of egg yolk and a linear consumption of perivitelline protein. EGGS EMBRYOS YOLK PERIVITELLINE PROTEIN MORPHOMETRY OCTOPODS ROBSOnella fOntaniana
316 I. URIARTE, O. ZUÑIGA, A. OLIVARES, V. ESPINOZA, V. CERNA, A. FARÍAS, C. ROSAS
Vie milieu, 2009, 59 (3-4)
tein content in the perivitelline liquid were quantified in an attempt to determine how the yolk absorption and the consumption of perivitelline protein are modulated dur-ing embryonic development and how they relate with embryonic growth.
MATERIAL AND METHODS
R. fontaniana females with eggs were collected
between November 2007 and November 2008 at Hueihe (41°52´S; 73°51´W), Region X, Chile. The octopuses and their spawn (attached to stones) were taken to the Marine Invertebrate Hatchery Laboratory of the Universidad Aus-tral de Chile (HIM-UACH) in 70-L tanks of aerated sea water. Once in the laboratory, the animals and stones with eggs were placed in individual aerated tanks of sea water kept at 12°C and 30 psu salinity; the tanks were connected to a sea water re-circulation system. The animals were placed in a semi-dark environment with a 12:12 h light: dark photoperiod and were fed daily with white fish (Odontestes sp.) to keep them from eating their spawn. Throughout embryonic development, the females sat on and cared for the spawn.
1. morphometric analyses and yolk quantification on the embryonic stages. We took samples (four eggs per day) from a
recent clutch using long forceps. These eggs were photographed, allowing us to study the embryonic anatomy over a period of 70 days. A total of 320 eggs and their corresponding embryos were measured and photographed using a light microscope (Stemi 2000-C) coupled to an AxioCam (ICc3; Zeiss) camera. The stages of embryonic development are defined according to Naef (1928) and the photos were used to determine morphometric relationships. For this, we measured egg length (EL), egg weight (EW), embryo total length (ETL), mantle length (ML), arm length (AL), and eye diameter (ED) during the same 70-day period (until hatching). The yolk sac volume was estimated by superimposing standard geometric forms onto the shape of the yolk sac. The anterior yolk sac, also called the outer yolk sac, was measured by superimposing ellipsoid, cylindrical, or spher-ical forms during embryonic development. The formulas used to determine the anterior yolk sac volume were:
i) Cylindrical volume (CV) = π r2 H
ii) Spherical volume (SV) = 4/3 π r3
where r is the ratio of the cylinder base or the ratio of the sphere, π is 3.1416, and H is the cylinder length. Yolk volumes were multiplied by a density of 1.036 mg mm-3 to convert them to wet
weights (Vidal et al. 2002).
An exponential equation was used to relate EL, ETL, AL, ML, and ED with octopus age (t):
morphological characteristic (mm) = a * ebt
where e is the base of the natural logarithm, the constants a and
b are the intercept and slope, and t is the age in days during
embryonic development. Other models were also adjusted to the morphological data as required (linear: Y = bX + a, or
logarith-mic: Y = a + b*ln(X), or allometric: Y = a*Xb; where Y is the
dependent variable and X is the independent variable).
2. Gravimetric analyses and quantification of the perivitell-ine protein. Seven clutches and their respective females were
collected from their natural environment during the year 2007-2008. Each clutch consisted of approximately 1700 eggs clus-tered in strands of 40 eggs. Two samples of 30 eggs were taken at random from each of the seven clutches, every 30 days, dur-ing embryonic development prior to hatchdur-ing; thus, a total of 1220 eggs were sampled. These eggs were measured individu-ally for length with a caliper (± 0.1 mm) and weighed on a Sar-torius analytical scale (± 0.0001 g). We calculated the age of the eggs from each clutch after hatching based on a 74-day-long embryonic period; this value was empirically obtained from eggs laid in our laboratory by a gravid female and reared at 12ºC under maternal care. Each sampled egg was punctured and its contents were emptied into a previously weighed Eppendorf tube. Once emptied, the 30 egg contents were centrifuged at 1000 rpm at 4ºC for 10 min, after which the supernatant corre-sponding to the perivitelline liquid of the 30 eggs was trans-ferred to a new, previously weighed Eppendorf tube, whereas the precipitate corresponding to the yolk plus the embryo was left in the original tube. Two aliquots (10 µl each) were taken from the perivitelline liquid and the soluble protein content was measured with a portable refractometer (Quimis, model Q-767-5 Serum Protein). Later, the perivitelline liquid and the yolk+embryo were freeze-dried in a SAVANT freeze-dryer (model Novalyphe-150) and weighed to determine their dry weight. We evaluated the growth rates of the eggs between the 30-day periods and related the change in perivitelline liquid pro-tein concentrations to the egg size and age.
RESULTS
Morphological relationships during embryonic development
Immediately after being laid (day 0), the central axis of the clutch was visible and the chorionic filaments of each egg were wrapped around this (Fig.1A). In stage I, the cleavage of the egg occurred at the animal pole where there was no yolk, thus forming a discoblastula. The rest of the cytoplasm did not divide (day 8). The polar bodies were found in the perivitelline space adjacent to the bor-der of the discoblastula (Fig. 1B). In stage VI, the rotary movement of the gastrula was evident (day 15). The blas-toderm cells had migrated to cover more than 50 % of the yolk surface (Fig. 1C). Once in stage IX (day 22), the embryo had rotated 180º, with its cephalic part at the base of the egg. The vitelline and the cephalic portions of the embryo could clearly be distinguished. In the latter por-tion, the formation of the mantle could be observed, along
Fig. 1. – Embryo development of R. fontaniana. A, Egg cluster at day 0; ca is central axis, chf are chorionic filaments. B, Stage I at day 8; d is discoblastula, pb are the polar bodies. C, Stage VI at day 15; bc are blastoderm cells and y is yolk surface. D, Stage IX at day 22; vp is vitelline portion, cp is cephalic portion, m is mantle, and r is retina. E, Stage XI at day 26; vs is vitelline sack, ra are rudimentary arms, e is eye, and m is mantle. F, Stage XV at day 50; chr are chromatophores, ivs is internal yolk sac and evs is external yolk sac. G, Stage XIX at day 61; evs is external yolk sac, chr a are arm chromatophores, and chr m are mantle chromatophores. H, Stage XX at day 71, ecd is a complete developed embryo, and ee is an empty egg.
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Vie milieu, 2009, 59 (3-4)
with the palleo visceral complex and the optical complex with the pigmentation of the retina (Fig. 1D). Later, in stage XI (day 26), the vitelline sac and the body of the embryo were clearly distinct. The rudimentary arms, the eye over the portion of the cranial complex, and the man-tle were easily identified (Fig. 1E). The first chromato-phores, both in the ventral and dorsal portions of the embryo, were formed in stage XV (day 50). At this point, the internal yolk sac was also organized in relation to the displacement of the external yolk (Fig. 1F). In stage XIX, the embryo had turned for the second time (day 61). The outer yolk sac was small and some content could remain between the arms, each of which had four
chromato-phores. Eight rows of chromatophores could be distin- guished on the back of the mantle (Fig. 1G). Once the embryo reached stage XX, it had completed its
develop-Fig. 2. – R. fontaniana clutch selected for morphometric analy-ses: relationships observed in 88 eggs between A, increased total egg length (EL) and egg age, B, increased egg weight (EW) and egg age, C, egg weight (EW) and egg length (EL), all for the entire period between laying and hatching. R2 is the coefficient
of determination and P indicates the significance of the coeffi-cient of regression.
Fig. 3. – R. fontaniana clutch selected for morphometric analy-ses: relationships observed between different embryonic organs and embryo age: A, increase in total embryo length (ETL); B, increase in mantle length (ML); C, increase in arm length (AL); and D, increase in eye diameter (ED). R2 is the coefficient of
determination and P indicates the significance of the coefficient of regression.
ment (day 71). It no longer had an external yolk sac and it was ready to hatch (Fig. 1H).
The length of the egg (EL) and its weight (EW) increased exponentially throughout the embryonic devel-opment (Fig. 2A, 2B). The weight of the egg was related allometrically to its length, with a slope of 2.41 (Fig. 2C).
An exponential relationship was obtained between embryo total length (ETL) and age (Fig. 3A). Similarly, exponential relationships were observed between ML and age and AL and age (Fig. 3B, 3C). Eye diameter showed a logarithmic curve with age; the maximum eye diameter for embryos was around 0.45 mm (Fig. 3D).
The yolk volume decreased exponentially during embryonic development (Fig. 4) such that, a few days prior to hatching, only 10 % of the external yolk remained available.
The length of the embryo was related exponentially to egg length (Fig. 5A). Both the mantle length (ML) and the arm length (AL) were related exponentially to the embryo length (Figs. 5B, 5C). The AL/ML ratio also showed a linear relationship with the total length of the embryo (Fig. 5D).
ML, as a proportion of ETL, increased with age between day 43 and day 54, reaching 76 to 92 % of ETL. Subsequently, the ML proportion declined and then remained at 73 % (days 57 to 64). Prior to hatching (day 69), ML was reduced to 67 % of ETL; this proportion was maintained until hatching (Fig. 6A). In contrast, arm length (AL) as a proportion of ETL decreased with age; values were high on day 43 (23 % of ETL) and low from days 50 to 57 (on average, 16 % of ETL). After day 57, AL in proportion to ETL returned to its initial value (around 23 %), remaining stable until hatching (Fig. 6B).
Gravimetric characterization
The eggs varied in size between the seven clutches observed and between the developmental stages within a
single clutch, ranging from 2.4 to 4.7 mm. In wet weight, this implied a variation between 2.9 and 8.0 mg. These two variables were related through an allometric equation
Fig. 4. – R. fontaniana clutch selected for morphometric analy-ses. Decrease in external egg yolk (EY) throughout the period of embryonic development. R2 is the coefficient of determination
and P indicates the significance of the coefficient of regression.
Fig. 5. – R. fontaniana clutch selected for morphometric analy-ses: relationship between A, embryo total length (ETL) and the total egg length (EL); B, mantle length (ML) and embryo total length (ETL); C, arm length (AL) and embryo total length (ETL); and D, ratio arm length/mantle length (AL/ML) and embryo total length (ETL). R2 is the coefficient of determination
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Vie milieu, 2009, 59 (3-4)
with a slope of 1.53. The eggs had specific growth rates of 0.0035 day-1 (± 0.0011; n = 5) for length and of 0.0096
day-1 (± 0.0021; n = 5) for wet weight, with no significant
differences between clutches. The protein content in the perivitelline liquid declined exponentially from 0.19 to 0.04 mg protein µL-1 (Fig. 7) with increased egg size. On
the other hand, the protein content in the perivitelline liq-uid decreased linearly (Fig. 8) with the increasing age of the embryos.
DISCUSSION
In this study, we have added a new growth phase in the life cycle of cephalopods – embryonic development – during which the growth rate for total length, mantle length, and arm length is also exponential, indicating that the type of growth described for paralarvae and juveniles begins during embryonic development.
The growth curve described for cephalopods is char-acterized by an initial exponential-type phase that lasts from the planktonic stage (where it exists) to the juvenile phase. After this, the growth is power-type until attain-ment sexual maturity (Van Heukelem 1973, Mangold 1983, Semmens et al. 2004, Leporati et al. 2007). Most morphometric information on embryos comes from
embryological studies of pre-hatching and hatched indi-viduals; these studies were reviewed by Boletzky (1977, 1989, 1994). However, to date, little of the data available has been used in an attempt to describe the allometric changes occurring during embryonic development in cephalopods.
During organogenesis, the cephalic organs (central nervous system and eyes) are the first conspicuous organs to appear in embryos because they are largely formed from ectodermic layers (Boletzky 2003). In the present study, cephalic organs were observed after day 22 (Stage IX, Fig. 1D) and well-defined eyes after day 26 (Stage XI, Fig. 1E). Our results for eye diameter indicate that, during embryonic development, the eyes grow following a loga-rithmic curve, suggesting that the cephalic organs form from ectodermic invaginations and grow rapidly at the beginning of embryonic development until organogenesis is completed. After that, during the planktonic post-hatch-ing stage, the growth of the cephalic organs follows an exponential curve (Uriarte et al. 2009). This suggests that the cephalic organs, once completed, follow a growth rate similar to that of the arms or mantle. According to
Villan-Fig. 6. – R. fontaniana clutch selected for morphometric analy-ses: A, variations in mantle length as a proportion of embryo total length (ML/ETL); and B, variations in the arm length as a proportion of embryo total length (AL/ETL), both throughout embryonic development. Different letters indicate significant differences in the ratio ML/ETL or AL/ETL between different embryo ages (Tukey HSD test; P < 0.05).
Fig. 7. – Decrease in perivitelline protein (PP) in relation to egg length (EL) for seven R. fontaniana clutches. Each point is an average of perivitellin protein (2 to 7 samples) per egg sizes between 2.8 and 4.3 mm. R2 is the coefficient of determination
and P indicates the significance of the coefficient of regression.
Fig. 8. – Variations in perivitelline protein (PP) as a function of the days of embryonic development for five R. fontaniana clutches of known ages. n = 2 samples per clutch at two differ-ent ages. R2 is the coefficient of determination and P indicates
ueva & Norman (2008), during paralarval stages, the pro-portion of the octopus mantle is greater than that of the arms. This shows that, during the first planktonic stages of growth, the organs located in the mantle cavity are more important than the arms. Results from the present study demonstrate that, although arms appear during early embryonic development (Boletzky 1984), the organs located in the mantle cavity determine the form in which the embryonic morphology is modulated. In fact, similar equations were obtained for the relationship between embryo total length vs. age (ETL = 0.38 e0.03 Age) and
man-tle length vs. age (ML = 0.30 e0.03 Age), indicating that,
dur-ing embryonic development, the total length is strongly influenced by mantle growth. According to Boletzky (2003), once the organogenesis of the cephalic organs starts, dramatic changes occur in the embryonic body, resulting in an increasingly compact arrangement of the organs, which take up their definitive position in the developing animal. An exponential increment in oxygen consumption by Sepia apama embryos could offer evi-dence of strong energy mobilization occurring during the exponential growth curve of this developmental stage (Cronin & Seymour 2000).
In the present study, during embryonic development, the proportion of R. fontaniana mantle and arms changed with age, with early mantle cavity growth followed by later arm growth. In fact, the mantle cavity reached nearly 95 % of the total embryonic length at day 54, indicating that, during that development time, the energy was chan-neled almost exclusively to organogenesis. In contrast, the proportion of the arms during embryonic development was between 15 and 24 %, peaking just before hatching. At this time, it seems that the post-hatching planktonic stage moved on to the second phase of development, in which the arms were the priority before settlement (Uri-arte et al. 2009).
R. fontaniana egg sizes fluctuated between 3.13 and
3.77 mm length in the clutch used for the descriptions and between 2.4 and 4.7 mm (3.5 and 6.8 % of adult ML, respectively) in the seven clutches used for gravimetric characterization (N = 1220). These eggs are considered to be small-type eggs (Boletzky 1977, Boletzky et al. 2002), comparable with those of the species O. bimaculatus (Hochberg et al. 1992) and O. mimus (Zuñiga et al. 1997); they fall within the range reported by Boletzky et al. (2002) for merobenthic octopodids (smaller than 10 % of adult ML). Variations in egg size can be explained by water uptake through the corion, the growth in length and weight throughout embryonic development, and differ-ences between clutches. Nevertheless, the influence of environmental factors and other characteristics of the females (age, size) were not measured in this work. The range of growth rates observed for the eggs from different clutches, both in size and in weight, perfectly encompass-es the growth observed in the eggs of the only clutch used for the morphological and morphometric descriptions.
The spring, summer, and autumn clutches did not differ significantly in their growth parameters during embryonic development, which was done under standardized condi-tions (12 ºC), so that the clutch selected for the first description was representative of the development of this species.
The entire R. fontaniana embryonic development took 71 to 76 days, until the paralarvae hatched. The clutch selected for the description contained recently laid and fertilized eggs, allowing us to describe the stages from the onset of segmentation (stage I) through the completion of development (stage XX). The embryos rotated twice: once at 19 days (stage IX) and again at 61 days (stage XIX). This is similar to observations for other octopuses (e.g. Ignatius & Srinivasan 2006; Kaneko et al. 2006). Such embryonic rotations in octopods correspond to dif-ferent phenomena. The first rotation, once dubbed blas-tokinesis, is due to cilia on the external part of the yolk sac that while changing direction of beat cause the embryo to rotate around its longitudinal axis. The second rotation, which occurs at the end of the embryonic development, compensates for this earlier inversion and grants the embryo a better position for hatching (Boletzky 1971, Lenz 1997).
In the present work, the hatching period for R.
fontani-ana lasted an average of 4 to 5 days at 12 ºC. The
hatch-ing period for a shatch-ingle clutch of eggs can be short (i.e., hours) or may last a few days or a period of weeks. It can be influenced by factors such as the length of the incuba-tion period of the eggs, the incubaincuba-tion temperature, and the species (Villanueva & Norman 2008). O. luteus hatch-es during 10 days at 18.2 to 20 ºC (Arakawa, 1962) and from 4 to 7 days at 21 to 27 ºC (Caveriviere et al. 1999), whereas O. vulgaris needs 9 days at 17 to 19 ºC (Iglesias
et al. 2004). For O. laqueus, on the other hand, 75 % of
the individuals that hatch do so within one hour on the same day (Kaneko et al. 2006).
The egg yolk was reduced exponentially during embry-onic development. Interestingly, the slope of these curves was negative (- 0.03), as compared to the slopes for the embryo total length and mantle length curves (0.03). This indicates that the decreasing velocity of yolk consump-tion was a direct consequence of the embryonic growth. The linear consumption of perivitelline protein during embryonic development could indicate that this protein is being used in morphogenesis. For gastropods, the perivi-telline fluid is consumed by the developing embryo as an energetic and structural source because it is mainly com-posed of lipoprotein (Garin et al. 1996), principally a lipoglycocarotenoprotein protecting the egg from oxida-tion (Dreon et al. 2004). The use of the protein in the perivitelline fluid has not been documented previously in octopuses.
According to those results, the use of yolk can be con-sidered as a source of energy for octopus development, and probably yolk and perivitelline protein contribute
322 I. URIARTE, O. ZUÑIGA, A. OLIVARES, V. ESPINOZA, V. CERNA, A. FARÍAS, C. ROSAS
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with protein and phospholipid for new cells during mor-phogenesis. So, the yolk and the protein in the perivitell-ine fluid could be used to monitor environmental effects or the egg quality on cephalopod clutches.
There is an inverse relationship between temperature and length of embryonic development in marine poikilo-therms, so when cephalopods are distributed at lower temperatures, their development times should be greater (Boletzky 1994, Johnston 1990, Naef 1928, Rocha et al 2001). For tropical species, reports show development takes 18 to 20 days for Octopus aegina incubated at 28 and 30 ºC (Ignatius & Srinivasan 2006); 21 days for
Octo-pus cyanea incubated at 27.1 ºC (Van Heukelem 1973);
22 to 25 days for Octopus vulgaris incubated at 25 ºC (Mangold 1983); 80 to 87 days for O. vulgaris incubated at 17 ºC (Caveriviere et al. 1999); and 23 days for
Wun-derpus photogenicus incubated at 26ºC (Miske &
Kirch-hauser 2006). In temperate-water species subjected to extreme temperature oscillations caused by El Niño Southern Oscillation (e.g., Octopus mimus off northern Chile; 17º30’S and 30ºS), embryonic development can be shortened to 65 % at 24º C (as compared to the normal upwelling temperature of 16 ºC) without deformations and maintaining hatching rates at 95 % (Warnke 1999). In contrast, species adapted to low temperatures have longer periods of embryonic development: eggs of the giant octopus enteroctopus dofleini are incubated for 161 days at 9.2 to 13.9º C (Gabe 1975), those of the chestnut octo-pus Octoocto-pus conispadiceus for 10 to 11 months between 2.2 and 17.2 ºC (Ito 1983); and eggs of the southern red octopus enteroctopus megalocyathus for 150 days at 12ºC (Uriarte et al. 2008). In the present study, R.
fontani-ana averaged 74 days of embryonic development at 12
ºC, indicating that its embryonic development is slower than that of the tropical species mentioned, but faster than that of the cold-water species of the genus enteroctopus.
Nonetheless, R. fontaniana is distributed from the north of Peru on the Pacific coast, stretching around Cape Horn at the extreme south of South America (56 ºS) and up to 41 ºS on the Atlantic coast (Ibañez et al. 2008). Therefore, this species is subjected to large fluctuations in the temperature of the sea water throughout its distribu-tion range. At its northern limit, it may be subjected to temperatures as high as 24 ºC due to the El Niño Southern Oscillation and in the far south of Chile, it may experi-ence temperatures below 5 ºC. Future research on this interesting species should include comparative studies of the reproductive conditioning of the specimens from the north and south of its distribution in order to determine how temperature changes along latitude modulate the duration of embryonic development, as well as other reproductive parameters of the species.
Acknowledgements. – This study was financed by
FOND-EF D04 I1401 and by the Excellency Research Net of CONI-CYT-World Bank ACI-34 Bicentennial Science and Technology Program, granted to I Uriarte. We also extend our
acknowledge-ments to J Hernández & R Miranda, who provided technical support.
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Received June 11, 2009 accepted december 1, 2009 associate editor: R Villanueva
